<br><br><div class="gmail_quote">---------- Forwarded message ----------<br>From: <b class="gmail_sendername">Neal Smith</b> <span dir="ltr"><<a href="mailto:smithn@stri.org">smithn@stri.org</a>></span><br>Date: Sun, Jul 25, 2010 at 4:57 PM<br>
Subject: CONSERVATION GENETICS OF NEOTROPICAL POLLINATORS REVISITED: MICROSATELLITE ANALYSIS SUGGESTS THAT DIPLOID MALES ARE RARE IN ORCHID BEES<br>To: Neal Smith <<a href="mailto:smithn@si.edu">smithn@si.edu</a>><br>
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<div><strong>SCIENCE SENDINGS!!</strong></div>
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<div><strong>NOTA BENE : I found this paper to be a difficult read
and decided that I was weak in the literature. So I attached pertinent PDF's
Roubik should be 1996. This paper is diploid orchid bees.. So this is
conservation genetics.........</strong></div>
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<h2><a href="http://www3.interscience.wiley.com/journal/117958524/home" target="_blank">Evolution</a></h2>
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<div>CONSERVATION GENETICS OF NEOTROPICAL POLLINATORS
REVISITED: MICROSATELLITE ANALYSIS SUGGESTS THAT DIPLOID MALES ARE RARE IN
ORCHID BEES</div></div>
<div><span><span>Rogério
O.</span> <span>Souza</span> <sup>1,2</sup>
</span>, <span><span>Marco A.</span> <span>Del Lama</span> <sup>1</sup> </span>, <span><span>Marcelo</span> <span>Cervini</span> <sup>3</sup> </span>, <span><span>Norma</span> <span>Mortari</span> <sup>3</sup> </span>, <span><span>Thomas</span> <span>Eltz</span> <sup>4</sup> </span>, <span><span>Yvonne</span> <span>Zimmermann</span> <sup>4</sup> </span>, <span><span>Carola</span> <span>Bach</span> <sup>4</sup> </span>, <span><span>Berry J.</span> <span>Brosi</span> <sup>5,6</sup> </span>, <span><span>Sevan</span> <span>Suni</span> <sup>7</sup> </span>, <span><span>J. Javier G.</span> <span>Quezada-Euán</span> <sup>8</sup> </span>, and
<span><span>Robert J.</span> <span>Paxton</span> <sup>9,10,11,12</sup> </span>
<div><span><a name="12a0b9da95851476_a1"> </a><span> <span><sup>1</sup> </span>Laboratório de Genética
Evolutiva de Himenópteros, Departamento de Genética e Evolução,
Universidade Federal de São Carlos, CEP 13565-905, São Carlos, São Paulo,
Brazil</span> <a name="12a0b9da95851476_a3"> </a><span>
<span><sup>3</sup> </span>Laboratório de
Imunogenética – DNA, Departamento de Genética e Evolução, Universidade
Federal de São Carlos, C.P. 676, CEP 13565-905, São Carlos, São Paulo,
Brazil</span> <a name="12a0b9da95851476_a4"> </a><span>
<span><sup>4</sup> </span>Sensory Ecology Group,
University of Düsseldorf, Universitätsstrasse 1, D-40225 Düsseldorf,
Germany</span> <a name="12a0b9da95851476_a5"> </a><span>
<span><sup>5</sup> </span>Department of Biology,
Stanford University, 385 Serra Mall, Stanford, California 94305</span> <a name="12a0b9da95851476_a7"> </a><span> <span><sup>7</sup> </span>Center for Insect Science,
University of Arizona, Tucson, Arizona 85721</span> <a name="12a0b9da95851476_a8"> </a><span> <span><sup>8</sup> </span>Departamento de Apicultura,
Universidad Autonoma de Yucatán, Mérida, Mexico</span> <a name="12a0b9da95851476_a9"> </a><span> <span><sup>9</sup> </span>School of Biological
Sciences, Queen's University Belfast, 97 Lisburn Road, Belfast BT9 7BL,
United Kingdom</span> <a name="12a0b9da95851476_a12"> </a><span> <span><sup>12</sup> </span>E-mail: <a href="mailto:rjp246@cornell.edu" target="_blank">rjp246@cornell.edu</a></span>
</span></div></div>
<div><span><span>Associate
Editor</span>: <span>C.</span> <span>Jiggins</span></span>
<div></div></div>
<div><a name="12a0b9da95851476_fn1"> </a>
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<p><span><sup>2</sup> </span>Present
Address: Universidade Federal do Acre, Estrada do Canela Fina Km 12,
Colônia São Francisco, Gleba Formoso Lote 245, Cruzeiro do Sul, CEP
69.980-000, Acre Brazil.</p></div><a name="12a0b9da95851476_fn2"> </a>
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<p><span><sup>6</sup>
</span>Department of Environmental Studies, Emory University, Math &
Science Center, Suite E510, 400 Dowman Drive, Atlanta, Georgia
3032.</p></div><a name="12a0b9da95851476_fn3"> </a>
<div>
<p><span><sup>10</sup>
</span>Department of Entomology, Cornell University, Comstock Hall,
Ithaca, New York 14853.</p></div><a name="12a0b9da95851476_fn4"> </a>
<div>
<p><span><sup>11</sup>
</span>Institute for Biology, Martin-Luther-University Halle-Wittenberg,
Hoher Weg 8, D-06099 Halle (Saale), Germany.</p></div></div>
<div>Copyright © 2010, Society for the Study of
Evolution</div></div>
<div>
<div>KEYWORDS</div>
<div>Complementary sex determination • <span>csd</span> • Euglossini • Hymenoptera</div></div>
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<h1>ABSTRACT</h1></div>
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<td><img title="Abstract" border="0" alt="Abstract" src="http://www3.interscience.wiley.com/images/sec_here_small.gif"></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2" target="_blank"><img title="Material and Methods" border="0" alt="Material and Methods" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
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<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6" target="_blank"><img title="LITERATURE CITED" border="0" alt="LITERATURE CITED" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
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<p>Allozyme analyses have suggested that Neotropical orchid bee
(Euglossini) pollinators are vulnerable because of putative high
frequencies of diploid males, a result of loss of sex allele diversity in
small hymenopteran populations with single locus complementary sex
determination. Our analysis of 1010 males from 27 species of euglossine
bees sampled across the Neotropics at 2–11 polymorphic microsatellite loci
revealed only five diploid males at an overall frequency of 0.005 (95% CIs
0.002–0.010); errors through genetic nondetection of diploid males were
likely small. In contrast to allozyme-based studies, we detected very weak
or insignificant population genetic structure, even for a pair of
populations >500 km apart, possibly accounting for low diploid male
frequencies. Technical flaws in previous allozyme-based analyses have
probably led to considerable overestimation of diploid male production in
orchid bees. Other factors may have a more immediate impact on population
persistence than the genetic load imposed by diploid males on these
important Neotropical pollinators.</p></div></div>
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<div><span>
<p>Received November 16, 2009<br>Accepted May 31,
2010</p></span></div>
<div>
<div>DIGITAL OBJECT IDENTIFIER (DOI)</div><span>10.1111/j.1558-5646.2010.01052.x</span> <a href="http://www3.interscience.wiley.com/doiinfo.html" target="_blank">About
DOI</a></div>
<div><a name="12a0b9da95851476_s1"> </a>
<div><a name="12a0b9da95851476_ss1"> </a>
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<div>Article Text</div>
<p>Single locus complementary sex determination (slCSD), in
which homozygosity at the sex locus leads to the production of effectively
sterile diploid (2N) males, is thought to be ancestral to the haplodiploid
Hymenoptera and has been considered widespread within the order (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b59" target="_blank">van
Wilgenburg et al. 2006</a>; but see <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b14" target="_blank">Cowan
and Stahlhut 2004</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b16" target="_blank">de
Boer et al. 2007, 2008</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b28" target="_blank">Heimpel
and de Boer 2008</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b60" target="_blank">Verhulst
et al. 2010</a>). The frequency of 2N males theoretically increases with
inbreeding, small population size, and reduced gene flow due to lack of
allelic diversity at the sex locus (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b11" target="_blank">Cook
1993</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b12" target="_blank">Cook
and Crozier 1995</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b59" target="_blank">van
Wilgenburg et al. 2006</a>). slCSD may itself lead to lower effective
population size (<span>N</span><sub>e</sub>) compared
to diploidy (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b62" target="_blank">Zayed
2004</a>).</p>
<p>All bees appear to be slCSD haplodiploids (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b59" target="_blank">van
Wilgenburg et al. 2006</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b63" target="_blank">Zayed
2009</a>) and there is growing evidence for decline in many groups (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b6" target="_blank">Brown
and Paxton 2009</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b44" target="_blank">Potts
et al. 2010</a>); unequivocal evidence is seen in solitary bees in England
and the Netherlands (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b3" target="_blank">Biesmeijer
et al. 2006</a>), bumblebees in Ireland (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b24" target="_blank">Fitzpatrick
et al. 2007</a>), and honey bees (<span>Apis mellifera</span>) in
the USA (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b36" target="_blank">Oldroyd
2007</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b57" target="_blank">vanEngelsdorp
et al. 2009</a>). This is cause for concern because bees are important
pollinators in natural and agro-ecosystems (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b31" target="_blank">Klein
et al. 2007</a>). Pollination is an important ecosystem service that is
being degraded by anthropogenic changes (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b32" target="_blank">Kremen
et al. 2002</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b53" target="_blank">Steffan-Dewenter
et al. 2005</a>), including habitat destruction, pollution, and
facilitation of invasive species (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b35" target="_blank">Mooney
et al. 2005</a>). Degradation of habitat may result in a loss of genetic
diversity, so the frequency of 2N males has been proposed to be a
sensitive measure of pollinator decline for bees (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65" target="_blank">Zayed
et al. 2004</a>). <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b64" target="_blank">Zayed
and Packer's (2005)</a> theoretical modeling concluded that diploid males
exert a high genetic load on populations, which could potentially drive a
genetic extinction vortex in slCSD haplodiploids.</p>
<p>The Euglossini comprise ca. 200 species of Neotropical bees
that are the sole pollinators of around 700 orchid species (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b19" target="_blank">Dressler
1982</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b7" target="_blank">Cameron
2004</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b48" target="_blank">Roubik
and Hanson 2004</a>). Males collect perfumes from orchid blossoms and
other sources in their hind tibiae and later release them at mating sites,
possibly to attract females (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b21" target="_blank">Eltz
et al. 2005, 2007</a>). To date the conservation genetics of orchid bees
has relied on the use of allozymes as genetic markers to study 2N male
frequency and determine ploidy (a male heterozygous at one or more loci is
a 2N male). An early study of seven Panamanian orchid bee species
suggested that 2N males comprised 12–100% of males per species (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49" target="_blank">Roubik
et al. 1996</a>). In contrast, <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55" target="_blank">Takahashi
et al. (2001)</a> found very low (mean 0–2% per species) frequencies of 2N
males in 14 Brazilian species. <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65" target="_blank">Zayed
et al. (2004)</a> subsequently detected 13–56% (across populations) of
Panamanian <span>Euglossa imperialis</span> males to be diploid
and inferred extremely limited gene flow and low <span>N</span><sub>e</sub> in the species, supporting <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49" target="_blank">Roubik
et al.'s (1996)</a> view that orchid bees exhibited low diversity at the
sex locus. More recently, <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b33" target="_blank">López-Uribe
et al. (2007)</a> also found high 2N male frequencies in five Colombian
orchid bee species; across species, 8–32% of males were estimated to be
diploid. Although all these studies employed substantial sample sizes
(<span>n</span>= 142–695 males per study), confidence intervals of
2N male frequencies were large due to the low variability of allozymes,
the only polymorphic markers then available for orchid bee population
genetics.</p>
<p>The notion that orchid bees suffer high 2N male production
is at odds with other aspects of the taxon's biology. For example, males
of many species are common at chemical baits and hence are employed in
Neotropical biodiversity inventorying (e.g., <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b5" target="_blank">Brosi
2009</a>) whereas both sexes are thought to be extremely mobile (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b29" target="_blank">Janzen
1971, 1981</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b19" target="_blank">Dressler
1982</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b7" target="_blank">Cameron
2004</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b17" target="_blank">Dick
et al. 2004</a>). This contradiction between biological observations and
allozyme-based genetic analysis prompted our re-assessment of 2N male
frequency and gene flow in orchid bees. Using three suites of recently
developed microsatellite markers, we genotyped 1010 males from 27 species
of euglossine bees, each at 2–11 polymorphic loci, sampled from across the
Neotropics and including <span>Eg. imperialis</span> from Panama,
to reveal extremely low (0.5%) frequencies of 2N males and very weak
population genetic structure even across 500 km.</p></div><a name="12a0b9da95851476_ss2"> </a>
<div><a name="12a0b9da95851476_h2"> </a>
<h1><span>Material and Methods</span> </h1>
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<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2" target="_blank"><img title="Material and Methods" border="0" alt="Material and Methods" src="http://www3.interscience.wiley.com/images/sec_here_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3" target="_blank"><img title="Results" border="0" alt="Results" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4" target="_blank"><img title="Discussion" border="0" alt="Discussion" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5" target="_blank"><img title="ACKNOWLEDGMENTS" border="0" alt="ACKNOWLEDGMENTS" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6" target="_blank"><img title="LITERATURE CITED" border="0" alt="LITERATURE CITED" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
</tr></tbody></table>
<p>In Brazil and Colombia, 483 males from 23 species were
collected across multiple years at odor baits (1,8-cineole, skatole and
vanillin) at 14 sites in seven Brazilian states and one site in Colombia
(<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1" target="_blank">Table
1</a>, <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#f1" target="_blank">Fig.
1</a>). These included 143 males already genotyped using allozymes and
reported by <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55" target="_blank">Takahashi
et al. (2001)</a>. In Panama, 257 males from three species were collected
at odor baits; <span>Eg. imperialis</span> was collected from
three sites across March–May 2005, <span>Eg. tridentata</span>
from two sites across 16 days in March-April 2006 (both at 1,8-cineole
baits) and <span>Euglossa hemichlora</span> from one site in
September 2007 (at p-dimethoxybenzene baits, <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#f1" target="_blank">Fig.
1</a>). In Mexico, 73 <span>Euglossa aff. viridissima</span> males
(the lineage with three mandibular teeth, 3D, to be described as a new
species; Eltz et al. unpubl. ms) and 57 <span>Eg.
viridissima</span> males (the lineage with two mandibular teeth, 2D; see
<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b23" target="_blank">Eltz
et al. 2008</a>) were collected at odor baits (p-dimethoxybenzene) from
one site in March 2006 and May 2007. Finally, in Costa Rica, 140 <span>Eulaema bombiformis</span> males were collected from 19 forest
fragments around Las Cruces Biological Station (maximum site separation
13.5 km) in June–September 2004, as described in <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b5" target="_blank">Brosi
(2009)</a>. Insects were stored in ethanol at −20°C or were dried and
stored at room temperature.</p><a name="12a0b9da95851476_t1"> </a>
<div>
<div>
<div>
<p><a name="12a0b9da95851476_t1_legend_span"> </a><span> <span><span>Table 1. </span> </span>Species name,
collection site, number of males sampled (<span>n</span> males),
number of polymorphic loci used (<span>n</span> loci), range of
expected intralocus allelic diversity (<span>H</span><sub>ina</sub>, adjusted for putative null
alleles; see Tables S1 and S2), mean allelic diversity across loci (<span>H</span><sub>exp</sub>, adjusted for putative null
alleles), probability of detecting a heterozygous male if diploid (<span>P</span><sub>het</sub>), observed number of diploid
(2N) males and 95% binomial confidence intervals of the observed frequency
of 2N males in 27 orchid bee species from Brazil, Colombia, Costa Rica,
Mexico, and Panama. See <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#f1" target="_blank">Figure
1</a> for sampling locations; Brazilian state codes are: Amazonas—AM;
Espírito Santo—ES; Minas Gerais—MG; Mato Grosso—MT; Paraíba—PB; Rio de
Janeiro—RJ; and São Paulo—SP.</span> </p></div></div>
<div align="center">
<table>
<tbody>
<tr valign="bottom">
<td>
<hr size="2" noshade>
</td></tr>
<tr>
<td align="middle">
<table>
<tbody>
<tr>
<th valign="bottom" align="left">Species</th>
<th valign="bottom" align="left">Collection Site</th>
<th valign="bottom" align="left"><span>n</span> males</th>
<th valign="bottom" align="left"><span>n</span> loci</th>
<th valign="bottom" align="left"><span>H</span>
<sub>ina</sub> </th>
<th valign="bottom" align="left"><span>H</span>
<sub>exp</sub> </th>
<th valign="bottom" align="left"><span>P</span>
<sub>het</sub> </th>
<th valign="bottom" align="left">2N males</th>
<th valign="bottom" align="left">95% CIs of 2N frequency</th></tr>
<tr>
<td valign="top" align="left"><span>Euglossa
annectans</span> </td>
<td valign="top" align="left">São Carlos – SP, Brazil</td>
<td valign="top" align="left">17*</td>
<td valign="top" align="left">6</td>
<td valign="top" align="left">0.17–0.75</td>
<td valign="top" align="left">0.48</td>
<td valign="top" align="left">0.988</td>
<td valign="top" align="left">1*</td>
<td valign="top" align="left">0.002–0.288</td></tr>
<tr>
<td valign="top" align="left"><span><span>Eg. chalybeata</span> </span></td>
<td valign="top" align="left"><span>Manaus – AM,
Brazil</span> </td>
<td valign="top" align="left"><span>19</span> </td>
<td valign="top" align="left"><span>6</span> </td>
<td valign="top" align="left"><span>0.28–0.72</span> </td>
<td valign="top" align="left"><span>0.60</span>
</td>
<td valign="top" align="left"><span>0.998</span>
</td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. cognata</span> </td>
<td valign="top" align="left">Villavicencio, Colombia</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left">9<sup>2</sup></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>Eg. cordata</span> </span></td>
<td valign="top" align="left"><span>Caraguatatuba
– SP, Brazil</span> </td>
<td valign="top" align="left"><span>37*</span> </td>
<td valign="top" align="left"><span>8</span> </td>
<td valign="top" align="left"><span>0.30–0.88</span> </td>
<td valign="top" align="left"><span>0.63</span>
</td>
<td valign="top" align="left"><span>>0.999</span> </td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"></td>
<td valign="top" align="left">São Carlos – SP, Brazil</td>
<td valign="top" align="left">30*</td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>Eg. fimbriata</span> </span></td>
<td valign="top" align="left"><span>São Carlos –
SP, Brazil</span> </td>
<td valign="top" align="left"><span>7*</span> </td>
<td valign="top" align="left"><span>8</span> </td>
<td valign="top" align="left"><span>0.25–0.86</span> </td>
<td valign="top" align="left"><span>0.56</span>
</td>
<td valign="top" align="left"><span>>0.999</span> </td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. hemichlora</span>
</td>
<td valign="top" align="left">Santa Rita, Panama</td>
<td valign="top" align="left">43</td>
<td valign="top" align="left">3</td>
<td valign="top" align="left">0.62–0.84</td>
<td valign="top" align="left">0.75</td>
<td valign="top" align="left">0.987</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>Manaus – AM,
Brazil</span> </td>
<td valign="top" align="left"><span>30</span> </td>
<td valign="top" align="left"><span>6</span> </td>
<td valign="top" align="left"><span>0.44–0.81</span> </td>
<td valign="top" align="left"><span>0.67</span>
</td>
<td valign="top" align="left"><span>>0.999</span> </td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. imperialis</span>
</td>
<td valign="top" align="left">Barro Colorado, Panama</td>
<td valign="top" align="left">47</td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>Fort Clayton,
Panama</span> </td>
<td valign="top" align="left"><span>23</span> </td>
<td valign="top" align="left"><span>5</span> </td>
<td valign="top" align="left"><span>0.02–0.83</span> </td>
<td valign="top" align="left"><span>0.45</span>
</td>
<td valign="top" align="left"><span>0.983</span>
</td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"></td>
<td valign="top" align="left">Gigante Peninsula, Panama</td>
<td valign="top" align="left">28</td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>Eg. intersecta</span> </span></td>
<td valign="top" align="left"><span>Manaus – AM,
Brazil</span> </td>
<td valign="top" align="left"><span>1</span> </td>
<td valign="top" align="left"><span>6<sup>2</sup></span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg.
mandibularis</span> </td>
<td valign="top" align="left">Viçosa – MG, Brazil</td>
<td valign="top" align="left">95*<sup>1</sup></td>
<td valign="top" align="left">8</td>
<td valign="top" align="left">0.08–0.87</td>
<td valign="top" align="left">0.56</td>
<td valign="top" align="left">>0.999</td>
<td valign="top" align="left">1*</td>
<td valign="top" align="left">0–0.057</td></tr>
<tr>
<td valign="top" align="left"><span><span>Eg. melanotricha</span> </span></td>
<td valign="top" align="left"><span>Analândia –
SP, Brazil</span> </td>
<td valign="top" align="left"><span>8*</span> </td>
<td valign="top" align="left"><span>9</span> </td>
<td valign="top" align="left"><span>0.38–0.88</span> </td>
<td valign="top" align="left"><span>0.66</span>
</td>
<td valign="top" align="left"><span>>0.999</span> </td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. mixta</span> </td>
<td valign="top" align="left">Villavicencio, Colombia</td>
<td valign="top" align="left">3</td>
<td valign="top" align="left">5</td>
<td valign="top" align="left">0.44–0.67</td>
<td valign="top" align="left">0.49</td>
<td valign="top" align="left">0.968</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>Eg. moure</span> </span></td>
<td valign="top" align="left"><span>Manaus – AM,
Brazil</span> </td>
<td valign="top" align="left"><span>1</span> </td>
<td valign="top" align="left"><span>7<sup>2</sup></span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. pleosticta</span>
</td>
<td valign="top" align="left">São Carlos – SP, Brazil</td>
<td valign="top" align="left">4*</td>
<td valign="top" align="left">9</td>
<td valign="top" align="left">0.38–0.75</td>
<td valign="top" align="left">0.63</td>
<td valign="top" align="left">>0.999</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>Camburí– SP,
Brazil</span> </td>
<td valign="top" align="left"><span>2</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. securigera</span>
</td>
<td valign="top" align="left">Rifaina – SP, Brazil</td>
<td valign="top" align="left">3</td>
<td valign="top" align="left">9</td>
<td valign="top" align="left">0.22–0.78</td>
<td valign="top" align="left">0.57</td>
<td valign="top" align="left">>0.999</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>São Carlos –
SP, Brazil</span> </td>
<td valign="top" align="left"><span>3*</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. townsendi</span>
</td>
<td valign="top" align="left">Araras – SP, Brazil</td>
<td valign="top" align="left">3</td>
<td valign="top" align="left">8</td>
<td valign="top" align="left">0.38–0.75</td>
<td valign="top" align="left">0.56</td>
<td valign="top" align="left">0.999</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>Rifaina – SP,
Brazil</span> </td>
<td valign="top" align="left"><span>1</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. tridentata</span>
</td>
<td valign="top" align="left">Barro Colorado, Panama</td>
<td valign="top" align="left">60</td>
<td valign="top" align="left">2</td>
<td valign="top" align="left">0.67–0.89</td>
<td valign="top" align="left">0.78</td>
<td valign="top" align="left">0.964</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left">0–0.049</td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>Parque Natur.
Metro., Panama</span> </td>
<td valign="top" align="left"><span>56</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. truncata</span>
</td>
<td valign="top" align="left">São Carlos – SP, Brazil</td>
<td valign="top" align="left">10*</td>
<td valign="top" align="left">7</td>
<td valign="top" align="left">0.42–0.78</td>
<td valign="top" align="left">0.65</td>
<td valign="top" align="left">>0.999</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>Eg. viridis</span> </span></td>
<td valign="top" align="left"><span>Villavicencio,
Colombia</span> </td>
<td valign="top" align="left"><span>1</span> </td>
<td valign="top" align="left"><span>9<sup>2</sup></span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eg. aff
viridissima</span> 3D<sup>3</sup></td>
<td valign="top" align="left">Xmatkuil, Mexico</td>
<td valign="top" align="left">73</td>
<td valign="top" align="left">2</td>
<td valign="top" align="left">0.85–0.89</td>
<td valign="top" align="left">0.87</td>
<td valign="top" align="left">0.984</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>Eg. viridissima</span>
2D<sup>4</sup></span> </td>
<td valign="top" align="left"><span>Xmatkuil,
Mexico</span> </td>
<td valign="top" align="left"><span>57</span> </td>
<td valign="top" align="left"><span>2</span> </td>
<td valign="top" align="left"><span>0.59–0.87</span> </td>
<td valign="top" align="left"><span>0.73</span>
</td>
<td valign="top" align="left"><span>0.948</span>
</td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eulaema</span> </td>
<td valign="top" align="left">Manaus – AM, Brazil</td>
<td valign="top" align="left">21</td>
<td valign="top" align="left">11</td>
<td valign="top" align="left">0.58–0.89</td>
<td valign="top" align="left">0.79</td>
<td valign="top" align="left">>0.999</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>bombiformis</span> </span></td>
<td valign="top" align="left"><span>Las Cruces,
Costa Rica</span> </td>
<td valign="top" align="left"><span>140</span> </td>
<td valign="top" align="left"><span>9</span> </td>
<td valign="top" align="left"><span>0.16–0.61</span> </td>
<td valign="top" align="left"><span>0.34</span>
</td>
<td valign="top" align="left"><span>0.981</span>
</td>
<td valign="top" align="left"><span>2</span> </td>
<td valign="top" align="left"><span>0–0.051</span>
</td></tr>
<tr>
<td valign="top" align="left"><span>El. cingulata</span>
</td>
<td valign="top" align="left">Manaus – AM, Brazil</td>
<td valign="top" align="left">8</td>
<td valign="top" align="left">7</td>
<td valign="top" align="left">0.47–0.81</td>
<td valign="top" align="left">0.63</td>
<td valign="top" align="left">>0.999</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>El. meriana</span> </span></td>
<td valign="top" align="left"><span>Manaus – AM,
Brazil</span> </td>
<td valign="top" align="left"><span>26</span> </td>
<td valign="top" align="left"><span>10</span> </td>
<td valign="top" align="left"><span>0.27–0.89</span> </td>
<td valign="top" align="left"><span>0.69</span>
</td>
<td valign="top" align="left"><span>>0.999</span> </td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"></td>
<td valign="top" align="left">Cuiabá– MT, Brazil</td>
<td valign="top" align="left">4</td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>Manaus – AM,
Brazil</span> </td>
<td valign="top" align="left"><span>4</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"></td>
<td valign="top" align="left">Marliéria – ES, Brazil</td>
<td valign="top" align="left">5</td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>Mimoso – MG,
Brazil</span> </td>
<td valign="top" align="left"><span>4</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>El. nigrita</span> </td>
<td valign="top" align="left">Poconé– MT, Brazil</td>
<td valign="top" align="left">3*</td>
<td valign="top" align="left">11</td>
<td valign="top" align="left">0.61–0.91</td>
<td valign="top" align="left">0.77</td>
<td valign="top" align="left">>0.999</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>Rifaina – SP,
Brazil</span> </td>
<td valign="top" align="left"><span>5</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"></td>
<td valign="top" align="left">S. J. Campos – SP, Brazil</td>
<td valign="top" align="left">5</td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>São Carlos –
SP, Brazil</span> </td>
<td valign="top" align="left"><span>5*</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"></td>
<td valign="top" align="left">Viçosa – MG, Brazil</td>
<td valign="top" align="left">5</td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>Eufriesea violacea</span> </span></td>
<td valign="top" align="left"><span>São Carlos –
SP, Brazil</span> </td>
<td valign="top" align="left"><span>16</span> </td>
<td valign="top" align="left"><span>10</span> </td>
<td valign="top" align="left"><span>0.37–0.85</span> </td>
<td valign="top" align="left"><span>0.59</span>
</td>
<td valign="top" align="left"><span>>0.999</span> </td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"></td>
<td valign="top" align="left">Viçosa – MG, Brazil</td>
<td valign="top" align="left">37</td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span><span>Exaerete frontalis</span> </span></td>
<td valign="top" align="left"><span>João Pessoa –
PB, Brazil</span> </td>
<td valign="top" align="left"><span>8</span> </td>
<td valign="top" align="left"><span>3</span> </td>
<td valign="top" align="left"><span>0.66–0.78</span> </td>
<td valign="top" align="left"><span>0.74</span>
</td>
<td valign="top" align="left"><span>0.983</span>
</td>
<td valign="top" align="left"><span>0</span> </td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Ex. smaragdina</span>
</td>
<td valign="top" align="left">João Pessoa – PB, Brazil</td>
<td valign="top" align="left">50</td>
<td valign="top" align="left">3</td>
<td valign="top" align="left">0.79–0.83</td>
<td valign="top" align="left">0.81</td>
<td valign="top" align="left">0.993</td>
<td valign="top" align="left">0</td>
<td valign="top" align="left"></td></tr>
<tr>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span>São Carlos –
SP, Brazil</span> </td>
<td valign="top" align="left"><span>1</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Grand Total</span> </td>
<td valign="top" align="left"></td>
<td valign="top" align="left"><span>1010</span> </td>
<td valign="top" align="left"></td>
<td valign="top" align="left"><span>0.02</span>–<span>0.91</span></td>
<td valign="top" align="left"><span>0.62</span> </td>
<td valign="top" align="left"><span>0.991</span> </td>
<td valign="top" align="left"><span>5</span> </td>
<td valign="top" align="left"><span>0.002–0.010</span>
</td></tr>
<tr valign="bottom">
<td colspan="9">
<hr size="1">
</td></tr>
<tr>
<td valign="bottom" colspan="9" align="left">*The same samples as
analyzed by <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55" target="_blank">Takahashi
et al. (2001)</a>;</td></tr>
<tr>
<td valign="bottom" colspan="9" align="left"><sup>1</sup> <span>n</span>=76
new samples added in addition to those of <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55" target="_blank">Takahashi
et al. (2001)</a>;</td></tr>
<tr>
<td valign="bottom" colspan="9" align="left"><sup>2</sup>For <span>n</span>=1 male analyzed, <span>n</span>
loci=number of loci employed (see Table S1);</td></tr>
<tr>
<td valign="bottom" colspan="9" align="left"><sup>3</sup>All males from the species
with three mandibular teeth, 3D (see <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b23" target="_blank">Eltz
et al. 2008</a>), to be described as a new species (Eltz et
al. unpubl. data).</td></tr>
<tr>
<td valign="bottom" colspan="9" align="left"><sup>4</sup>All males from the species
with two mandibular teeth, 2D (see <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b23" target="_blank">Eltz
et al. 2008</a>).</td></tr></tbody></table></td></tr>
<tr valign="bottom">
<td>
<hr size="2" noshade>
</td></tr></tbody></table></div></div>
<p> </p><a name="12a0b9da95851476_f1"> </a>
<div align="center">
<table border="0" width="85%">
<tbody>
<tr>
<td valign="top" width="128" align="left"><a><img border="0" src="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/tf1"></a></td>
<td align="left">
<div>
<p><a name="12a0b9da95851476_f1_legend_span"> </a><span> <span><span>Figure 1. </span> </span>Map of the
Neotropics with the 22 sampling sites highlighted as dots (five
adjacent localities in Panama are given one dot).</span>
</p></div><span>[<a>Normal View</a>
]</span></td></tr></tbody></table></div>
<p>DNA was extracted from legs or thoraxes using a high salt
protocol (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b40" target="_blank">Paxton
et al. 1996</a>) or a DNeasy Blood and Tissue Kit (Qiagen, Valencia,
California) following manufacturer's recommendations. Individuals were
genotyped at 2–11 polymorphic microsatellite loci (male
haplotypes/genotypes in Table S1), developed for <span>Euglossa
cordata</span>, <span>Eulaema nigrita</span> (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b52" target="_blank">Souza
et al. 2007</a>), and <span>Euglossa annectans</span> (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b42" target="_blank">Paxton
et al. 2009</a>); these are unlinked loci that are in Hardy–Weinberg
equilibrium (HWE) in the species for which they were developed (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b52" target="_blank">Souza
et al. 2007</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b42" target="_blank">Paxton
et al. 2009</a>). Genotyping and scoring were performed using
autosequencers in three different laboratories (Megabace 750, ABI 310, or
ABI 3100) and Genotyper or GeneMarker Version 1.71 software with internal
size standards. All trace files were inspected by eye to check for
potential allele miscalling due, for example, to stutter. Approximately 5%
of individuals were re-amplified and alleles scored using the same
autosequencer or they were genotyped in a fourth laboratory by
radio-labeling and resolving on manual sequencing gels (methods in <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b68" target="_blank">Paxton
et al. 1996</a>). Allele calling across these duplicate analyses of the
same individual-locus combination was identical. We therefore estimate
extremely low genotyping error rates.</p>
<p>Nondetection of 2N males may arise if genetic markers
exhibit low allelic diversity (low heterozygosity). To compensate for
genetic nondetection, we calculated the resolving power of our markers,
namely the probability that a diploid individual was heterozygous at one
or more loci, <span>P</span><sub>het</sub>, as <span><span><img alt="" src="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/eqm1">
</span><span></span></span>where summation is across
the <span>N</span> alleles at a locus and multiplication is across
<span>L</span> loci. This assumes HWE, although moderate levels of
inbreeding have only a slight effect on <span>P</span><sub>het</sub> (e.g., see <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b41" target="_blank">Paxton
et al. 2000</a>). In estimating allelic frequencies, males carrying only
one allele at all loci were considered haploid, which is a close
approximation given the high allelic diversity of the loci and therefore
the high probability that a diploid male is heterozygous at one or more
loci (Tables S1 and S2). In addition, microsatellite analysis of four of
our study species has not revealed any deviation from HWE (<span>Eg. annectans</span> in <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b42" target="_blank">Paxton
et al. 2009</a>; <span>Eg. cordata</span> and <span>El.
nigrita</span> in <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b52" target="_blank">Souza
et al. 2007</a>; and <span>Eg. viridissima</span> in <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b67" target="_blank">Zimmermann
et al. 2009</a>), suggesting random mating in orchid bees.</p>
<p>Null alleles can nevertheless cause difficulties in
microsatellite allele scoring and lead to an overestimation of <span>P</span><sub>het</sub>. To account for putative null
alleles, we assumed that a male lacking an allele at a locus was caused by
a null allele, and we reduced allelic diversity (<span>H</span><sub>ina</sub>) and <span>P</span><sub>het</sub> at that locus accordingly
(Table S1). We also analyzed females from seven of the 27 species at the
same loci as males of the respective species (Table S2). As female
euglossines are not attracted to odor baits and are therefore far more
difficult to sample than males, we did not have access to females of the
other 20 species. Of the seven species with females, <span>n</span> > 20 females for 5 species. Their genotypes were
tested for the presence of null alleles using MICRO-CHECKER (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b58" target="_blank">van
Oosterhout et al. 2004</a>) and we reduced allelic diversity (<span>H</span><sub>ina</sub> or expected heterozygosity
accounting for null alleles) and <span>P</span><sub>het</sub> for the three loci showing
evidence of null alleles using equation (4) of <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b4" target="_blank">Brookfield</a>
(1996; see Table S2). For the other loci, we calculated expected allelic
diversity (<span>H</span><sub>ina</sub> or expected
heterozygosity) from female genotypes using GENEPOP (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b45" target="_blank">Raymond
and Rousset 1995</a>). We conservatively used the lowest estimates of
<span>H</span><sub>ina</sub> and <span>P</span><sub>het</sub> derived from males or females
for each species-locus combination. Binomial 95% confidence intervals
(2-tailed) of the proportion of diploid males were calculated using J.C.
Pezzullo's Interactive Stats javascript (<a href="http://statpages.org/confint.html" target="_blank">http://statpages.org/confint.html</a>).</p>
<p>Four species were collected at two or more sites spanning
4–538 km: <span>Eg. cordata</span> (two sites), <span>Eg.
imperialis</span> (three sites), <span>Eg. tridentata</span> (two
sites), and <span>Eufriesea violacea</span> (two sites; see <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2" target="_blank">Table
2</a>) and genotyped in the same laboratory. For each population pair, we
computed estimates of genetic differentiation to infer population
connectivity. Both <span>F</span><sub>ST</sub> and <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b26" target="_blank">Hedrick's
(2005)</a> unbiased estimator of population differentiation, <span>G</span><sub>ST</sub>', were calculated with MSA
version 4.05 (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b18" target="_blank">Dieringer
and Schlötterer 2003</a>) using the male dataset as MSA can simultaneously
handle both haploid and diploid data. The significance of differentiation
measures was determined using an exact test with 1000 permutations in
MSA.</p><a name="12a0b9da95851476_t2"> </a>
<div>
<div>
<div>
<p><a name="12a0b9da95851476_t2_legend_span"> </a><span> <span><span>Table 2. </span> </span>Geographic
distances between pairs of populations of orchid bees (males) and genetic
differentiation measured as <span>F</span><sub>ST</sub> and <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b26" target="_blank">Hedrick's
(2005)</a> <span>G</span><sub>ST</sub>', with
exact <span>P</span> values (1000 permutations) from MSA (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b18" target="_blank">Dieringer
and Schlötterer 2003</a>). For locations, see <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#f1" target="_blank">Figure
1</a>.</span> </p></div></div>
<div align="center">
<table>
<tbody>
<tr valign="bottom">
<td>
<hr size="2" noshade>
</td></tr>
<tr>
<td align="middle">
<table>
<tbody>
<tr>
<th valign="bottom" align="left">Pair of populations</th>
<th valign="bottom" align="left"><span>n</span> (males)</th>
<th valign="bottom" align="left"><span>n</span> (loci)</th>
<th valign="bottom" align="left">Distance (km)</th>
<th valign="bottom" align="left"> <span>F</span><sub>ST</sub> (<span>P</span>)</th>
<th valign="bottom" align="left"><span>G</span>
<sub>ST</sub>' (<span>P</span>)</th></tr>
<tr>
<td valign="top" align="left"><span>Euglossa
cordata</span> (Brazil)</td>
<td valign="top" align="left">37</td>
<td valign="top" align="left">8</td>
<td valign="top" align="left">310</td>
<td valign="top" align="left"> 0.024 (0.005)</td>
<td valign="top" align="left">0.175 (0.037)</td></tr>
<tr>
<td valign="top" align="left"><span>Caraguatatuba
versus São Carlos</span> </td>
<td valign="top" align="left"><span>30</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Euglossa
imperialis</span> (Panama)</td>
<td valign="top" align="left">47</td>
<td valign="top" align="left">5</td>
<td valign="top" align="left">34</td>
<td valign="top" align="left"> 0.012 (0.176)</td>
<td valign="top" align="left">0.014 (0.827)</td></tr>
<tr>
<td valign="top" align="left"><span>Barro Colorado
versus Fort Clayton</span> </td>
<td valign="top" align="left"><span>23</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Euglossa
imperialis</span> (Panama)</td>
<td valign="top" align="left">47</td>
<td valign="top" align="left">5</td>
<td valign="top" align="left">4</td>
<td valign="top" align="left">−0.011 (0.767)</td>
<td valign="top" align="left">0.096 (0.422)</td></tr>
<tr>
<td valign="top" align="left"><span>Barro Colorado
versus Gigante Penninsula</span> </td>
<td valign="top" align="left"><span>28</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Euglossa
imperialis</span> (Panama)</td>
<td valign="top" align="left">23</td>
<td valign="top" align="left">5</td>
<td valign="top" align="left">32</td>
<td valign="top" align="left"> 0.004 (0.308)</td>
<td valign="top" align="left">0.038 (0.710)</td></tr>
<tr>
<td valign="top" align="left"><span>Fort Clayton
versus Gigante Penninsula</span> </td>
<td valign="top" align="left"><span>28</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Euglossa
tridentata</span> (Panama)</td>
<td valign="top" align="left">60</td>
<td valign="top" align="left">2</td>
<td valign="top" align="left">36</td>
<td valign="top" align="left"> 0.001 (0.354)</td>
<td valign="top" align="left">0.072 (0.379)</td></tr>
<tr>
<td valign="top" align="left"><span>Barro Colorado
versus Parque Natural Metropolitano</span> </td>
<td valign="top" align="left"><span>56</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr>
<tr>
<td valign="top" align="left"><span>Eufriesea
violacea</span> (Brazil)</td>
<td valign="top" align="left">16</td>
<td valign="top" align="left">10</td>
<td valign="top" align="left">538</td>
<td valign="top" align="left">−0.025 (0.991)</td>
<td valign="top" align="left">0.074 (0.598)</td></tr>
<tr>
<td valign="top" align="left"><span>São Carlos
versus Viçosa</span> </td>
<td valign="top" align="left"><span>37</span> </td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td>
<td valign="top" align="left"><span> </span>
</td></tr></tbody></table></td></tr>
<tr valign="bottom">
<td>
<hr size="2" noshade>
</td></tr></tbody></table></div></div>
<p> </p></div><a name="12a0b9da95851476_ss3"> </a>
<div><a name="12a0b9da95851476_h3"> </a>
<h1><span>Results</span> </h1>
<table>
<tbody>
<tr>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract" target="_blank"><img title="Abstract" border="0" alt="Abstract" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2" target="_blank"><img title="Material and Methods" border="0" alt="Material and Methods" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3" target="_blank"><img title="Results" border="0" alt="Results" src="http://www3.interscience.wiley.com/images/sec_here_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4" target="_blank"><img title="Discussion" border="0" alt="Discussion" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5" target="_blank"><img title="ACKNOWLEDGMENTS" border="0" alt="ACKNOWLEDGMENTS" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6" target="_blank"><img title="LITERATURE CITED" border="0" alt="LITERATURE CITED" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
</tr></tbody></table>
<p>Allelic diversity accounting for null alleles (expected
heterozygosity) of our loci, <span>H</span><sub>ina</sub>, ranged from 0.02 to 0.96 (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1" target="_blank">Table
1</a>). It was generally above 0.5 for most loci in most species (Tables
S1 and S2) and averaged 0.62 (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1" target="_blank">Table
1</a>). <span>H</span><sub>ina</sub> differed little
between males and females; it was greater by 0.044 in males versus females
(<span>n</span>= 5 species and <span>n</span>= 26
locus-species combinations), suggesting that our estimates of <span>P</span><sub>het</sub> in species for which we did
not sample females are only slightly inflated. Using 2–11 loci per species
gave an average <span>P</span><sub>het</sub> of 0.991
(range 0.948 to >0.999), sufficient resolving power to detect the
majority of diploid males as heterozygotes at one or more loci.</p>
<p>We detected five heterozygotes among the 1010 males that we
genotyped, one each in <span>Eg. annectans</span>, <span>Eg. mandibularis</span>, and <span>Eg. tridentata</span>,
and two in <span>El. bombiformis</span> (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1" target="_blank">Table
1</a>). The <span>Eg. mandibularis</span> male heterozygous at
microsatellite locus Egc24 (Table S1) was the same individual that <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55" target="_blank">Takahashi
et al. (2001)</a> also detected by allozyme analysis as a heterozygote. We
additionally detected one heterozygous <span>Eg. annectans</span>
male (heterozygous at loci Egc18 and Egc24; see Table S1) that <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55" target="_blank">Takahashi
et al. (2001)</a> found to be homozygous by allozyme analysis. Over all
males, and accounting for genetic nondetection errors (i.e., where <span>P</span><sub>het</sub> < 1), diploid male
frequency averaged 0.005 (95% CI's 0.002–0.010).</p>
<p>Population differentiation in orchid bees was generally
small and nonsignificant (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2" target="_blank">Table
2</a>), suggesting considerable gene flow. For the <span>Eg.
imperialis</span> dataset comprising three Panamanian populations 4–34 km
apart, global <span>F</span><sub>ST</sub>= 0.001
(<span>P</span>= 0.384) and <span>G</span><sub>ST</sub>'= 0.034 (<span>P</span>= 0.786). Pairwise measures of <span>Eg.
imperialis</span> population differentiation were similarly not
significantly different from zero (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2" target="_blank">Table
2</a>). The two <span>Eg. tridentata</span> populations separated
by 36 km were also not significantly differentiated (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2" target="_blank">Table
2</a>). The two <span>Eg. cordata</span> populations separated by
310 km showed low, though significant, estimates of <span>F</span><sub>ST</sub> and <span>G</span><sub>ST</sub>' (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2" target="_blank">Table
2</a>). In contrast, the two <span>Ef. violacea</span> populations
separated by 538 km were not significantly differentiated (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2" target="_blank">Table
2</a>), suggesting considerable gene flow between them.</p></div><a name="12a0b9da95851476_ss4"> </a>
<div><a name="12a0b9da95851476_h4"> </a>
<h1><span>Discussion</span> </h1>
<table>
<tbody>
<tr>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract" target="_blank"><img title="Abstract" border="0" alt="Abstract" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2" target="_blank"><img title="Material and Methods" border="0" alt="Material and Methods" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3" target="_blank"><img title="Results" border="0" alt="Results" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4" target="_blank"><img title="Discussion" border="0" alt="Discussion" src="http://www3.interscience.wiley.com/images/sec_here_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5" target="_blank"><img title="ACKNOWLEDGMENTS" border="0" alt="ACKNOWLEDGMENTS" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6" target="_blank"><img title="LITERATURE CITED" border="0" alt="LITERATURE CITED" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
</tr></tbody></table>
<p>We found strong evidence for extremely low frequencies of
diploid males among common and widespread orchid bees of the Neotropics.
Our broad taxonomic sampling from across a wide geographic area lends
weight to our analyses, while consistency in genotyping at four
independent laboratories and low estimated frequencies of null alleles
mean that the low 2N male frequencies we detected are unlikely to be a
technical artifact. We found little or no population genetic structure
over 10s–100s km; these results imply high gene flow, as also suggested by
a mitochondrial DNA-based phylogeography of orchid bees (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b17" target="_blank">Dick
et al. 2004</a>), which could explain the apparently adequate sex allele
diversity in orchid bees. Both low 2N male frequency and weak population
genetic structure suggest that many orchid bees have both high gene flow
and high <span>N</span><sub>e</sub>, and that they do
not suffer from inbreeding through genetic drift and loss of <span>csd</span> diversity.</p>
<p>Why is there a discrepancy between our microsatellite-based
study and all but one of the earlier allozyme-based studies demonstrating
high 2N male frequencies, high population viscosity, and low <span>N</span><sub>e</sub> (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49" target="_blank">Roubik
et al. 1996</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65" target="_blank">Zayed
et al. 2004</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b33" target="_blank">López-Uribe
et al. 2007</a>)? We offer two explanations.</p>
<p>First, high frequencies of diploid males might be site or
species-specific, and our sampling may not have captured sites or orchid
bee species with high 2N males revealed by earlier allozyme-based studies.
However, we analyzed males from four of the seven Panamanian species
reported by <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49" target="_blank">Roubik
et al. (1996)</a> that exhibited high 2N male frequencies (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49" target="_blank">Roubik
et al. 1996</a>, their <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1" target="_blank">Table
1</a>), and we included two species (<span>Eg. imperialis</span>
and <span>Eg. tridentata</span>) from the same sampling sites as
<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49" target="_blank">Roubik
et al. (1996)</a>. Furthermore, we did not detect any 2N males among the
98 <span>Eg. imperialis</span> males that we analyzed (95% CI's
0–3.8%) from the same three sampling sites at which <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65" target="_blank">Zayed
et al. (2004)</a> found 37.7% of <span>Eg. imperialis</span> males
to be 2N. It is therefore unlikely that our sampling scheme was
responsible for the discrepancies between our results and those of
previous studies. A caveat of our interpretation is that diploid males may
be produced during a specific season of the year, a period when <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49" target="_blank">Roubik
et al. (1996)</a> and <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65" target="_blank">Zayed
et al. (2004)</a> sampled but we did not.</p>
<p>Second, allozyme-based genotyping can suffer from allele
misscoring, possibly due to protein instability, whereas DNA is more
stable and therefore microsatellite genotyping more robust (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b50" target="_blank">Schlötterer
2004</a>). This may have resulted in an artificial excess of male
heterozygotes in allozyme studies; positive controls (diploid females)
were generally lacking in allozyme-based studies. Our microsatellite loci
detected high heterozygosity in females whenever they were available for
analysis (<span>Eg. annectans</span> in <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b42" target="_blank">Paxton
et al. 2009</a>; <span>Eg. cordata</span> and <span>El.
nigrita</span> in <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b52" target="_blank">Souza
et al. 2007</a>; <span>Euglossa igniventris</span>, T. Eltz,
unpubl. data; <span>EG. hemichlora</span>, <span>Eg.
townsendi</span>, <span>Eg. viridissima</span>, and <span>Exaerete smaragdina</span> in Table S2) and yet frequencies of
putative null alleles, a potential cause of microsatellite allele
miscalling that may lead to an underestimate of 2N male frequency, were
low. As we sampled females from only five of the 27 study species in
sufficient number to test statistically for null alleles, we urge caution
in the interpretation of our results, pending analysis of females from
additional species. We nevertheless conclude that allozyme-based studies
of orchid bees are probably methodologically flawed due to allele
misscoring, and that this flaw accounts for the differences between
allozyme-based studies and our microsatellite-based study. More direct
methods of assessing diploid male frequencies and including analysis of
females, for example by karyotype analysis (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b20" target="_blank">Eltz
et al. 1998</a>) or genome size estimation by flow cytometry (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b1" target="_blank">Aron
et al. 2005</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b13" target="_blank">Cournault
and Aron 2009</a>), are needed to support our microsatellite-based
conclusions.</p>
<p>Our interpretation of orchid bee population genetics, that
they have low 2N male production, very weak population structure, high
gene flow, and high <span>N</span><sub>e</sub>, fits
with many independent observations of the taxon. First, individual orchid
bees have been reported to travel long distances (>20 km; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b29" target="_blank">Janzen
1971</a>). Second, other orchid bee species are common faunal elements in
natural and disturbed habitats (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b5" target="_blank">Brosi
2009</a>) and even in urban centers (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b34" target="_blank">López-Uribe
et al. 2008</a>). Third, census data suggest that orchid bee abundance and
diversity appear to have been maintained (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b47" target="_blank">Roubik
2001</a>), even within the highly fragmented Atlantic rainforest of Brazil
(<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b56" target="_blank">Tonhasca
et al. 2002</a>). Finally, results from the phylogeographic study of <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b17" target="_blank">Dick
et al. (2004)</a> suggest that high gene flow across the South American
continent is characteristic of many orchid bee species. These behavioral
and genetic lines of evidence support the view that orchid bee populations
are large, weakly structured and unlikely to suffer from inbreeding
through loss of sex allele diversity.</p>
<p>Clearly, orchid bees may not be an informative test case of
the idea that 2N male frequencies are a sensitive measure of bee
pollinator decline (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65" target="_blank">Zayed
et al. 2004</a>) as they seem to exhibit high mobility and high allelic
diversity at the sex locus. For other bees, inbreeding is not necessarily
associated with high frequencies of 2N males as detected by
microsatellites (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b41" target="_blank">Paxton
et al. 2000</a>). Also, severely bottlenecked populations of the sweat bee
<span>Lasioglossum leucozonium</span> with high 2N male
frequencies detected by microsatellite genotyping have recently expanded
across Eastern USA (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b66" target="_blank">Zayed
et al. 2007</a>), suggesting that high 2N male frequencies are not
necessarily correlated with population decline in this invasive species.
Yet for the honey bee (<span>A. mellifera</span>) with a
well-characterized system of sex determination based on slCSD (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b2" target="_blank">Beye
et al. 2003</a>), high frequencies of 2N males have a catastrophic effect
on colony survival (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b61" target="_blank">Woyke
1980</a>), as in other social bees (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b43" target="_blank">Plowright
and Pallett 1979</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b8" target="_blank">Carvalho
2001</a>) and ants (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b46" target="_blank">Ross
and Fletcher 1986</a>). An appropriate test of the diploid male extinction
vortex (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b64" target="_blank">Zayed
and Packer 2005</a>) and the idea that the frequency of 2N males is a
sensitive measure of pollinator decline (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65" target="_blank">Zayed
et al. 2004</a>) awaits analysis of slCSD populations at their range
margins or of those that have been anthropogenically compromised. Eusocial
Hymenoptera such as bumblebees (e.g., <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b54" target="_blank">Takahashi
et al. 2008</a>) may be more suitable subjects for such a test than the
largely solitary and subsocial orchid bees (cf. <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b10" target="_blank">Cocom
Pech et al. 2008</a>) because hymenopteran eusociality is associated with
reduced genetic diversity and low <span>N</span><sub>e</sub> (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b38" target="_blank">Pamilo
et al. 1978, 1997</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b25" target="_blank">Graur
1985</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b27" target="_blank">Hedrick
and Parker 1997</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b9" target="_blank">Chapman
and Bourke 2001</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b37" target="_blank">Packer
and Owen 2001</a>).</p>
<p>Although bees are thought to possess slCSD (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b59" target="_blank">van
Wilgenburg et al. 2006</a>), the presence of a different kind of sex
determination in orchid bees could explain the observed low frequencies of
2N males. A parasitoid hymenopteran has recently been shown to possess
multilocus CSD (mlCSD; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b15" target="_blank">de
Boer et al. 2008</a>) and diploid males in hymenopterans with regular
inbreeding produce fertile diploid males (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b16" target="_blank">de
Boer et al. 2007</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b13" target="_blank">Cournault
and Aron 2009</a>); in one wasp with regular inbreeding, diploid males may
even produce haploid sperm (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b14" target="_blank">Cowan
and Stahlhut 2004</a>). Sex determination through genomic imprinting has
also been recently demonstrated in the haplodiploid hymenopteran <span>Nasonia</span> (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b60" target="_blank">Verhulst
et al. 2010</a>). The presence of occasional diploid males in otherwise
haploid-male orchid bees indicates that the taxon possesses CSD. The low
frequency of 2N males that we observed may be a consequence of mlCSD.</p>
<p>Our sampling of 26 orchid bee species from across a wide
geographic range and habitat types (coastal Atlantic forest, cerrado open
woodland, Amazonian tropical forest), including sites with old-growth
vegetation (Barro Colorado Island) and others with highly disturbed
vegetation (e.g., São Carlos; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b51" target="_blank">Soares
et al. 2003</a>), allow us to draw conclusions concerning the conservation
genetics of this taxon. First, orchid bees currently appear to have
extremely low frequencies of 2N males, suggesting that continental
populations are probably not prone to the diploid male extinction vortex
(<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b64" target="_blank">Zayed
and Packer 2005</a>), possibly because of high gene flow maintaining
adequate allelic diversity at the sex locus. Second, they appear to be
highly mobile, again increasing <span>N</span><sub>e</sub> beyond those predicted from
estimates of census size at one point in time and space. Nevertheless, we
urge caution in the generalization of our results. Morphological
similarity among orchid bees (<a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b48" target="_blank">Roubik
and Hanson 2004</a>; <a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b23" target="_blank">Eltz
et al. 2008</a>) may hide cryptic species diversity, and rare species or
isolated populations at range margins may yet be found to suffer the
genetic load of high diploid male production.</p></div></div><a name="12a0b9da95851476_s2"> </a>
<div>
<div><span><span>Associate
Editor</span>: <span>C.</span> <span>Jiggins</span></span>
<div></div></div><a name="12a0b9da95851476_ss5"> </a>
<div><a name="12a0b9da95851476_h5"> </a>
<h1>ACKNOWLEDGMENTS</h1>
<table>
<tbody>
<tr>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract" target="_blank"><img title="Abstract" border="0" alt="Abstract" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2" target="_blank"><img title="Material and Methods" border="0" alt="Material and Methods" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3" target="_blank"><img title="Results" border="0" alt="Results" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4" target="_blank"><img title="Discussion" border="0" alt="Discussion" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5" target="_blank"><img title="ACKNOWLEDGMENTS" border="0" alt="ACKNOWLEDGMENTS" src="http://www3.interscience.wiley.com/images/sec_here_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6" target="_blank"><img title="LITERATURE CITED" border="0" alt="LITERATURE CITED" src="http://www3.interscience.wiley.com/images/sec_down_small.gif"></a></td>
</tr></tbody></table>
<p>We thank J. C. Serrano and E. J. dos Anjos Silva for species
identification; M. M. López-Uribe, C. A. Oi, and D. W. Roubik for help in
sampling; and EMBRAPA Pecuária Sudeste, Parque Ecológico de São Carlos and
Canil Municipal de São Carlos for permission to sample bees in their
areas. We also thank M. M. López-Uribe, the reviewers and associate editor
for helpful comments on the manuscript. Our special thanks go to IBAMA
(Dr. Helena K. Boscolo) for the license to collect and transport material;
to the members of Universidade Federal de São Carlos and Queen's
University Belfast for support; to CNPq (Edital Universal 475935/04-7),
CNPq (# 142131/03-2) and CAPES (BEX-218204/1) for a scholarship to ROS;
and to the Deutsche Forschungsgemeinschaft (EL 249-3) and the
CONACYT-European Union cooperative project of FONCICYT (MUTUAL: grant #
94293) for current funding.</p></div><a name="12a0b9da95851476_ss6"> </a>
<div><a name="12a0b9da95851476_h6"> </a>
<h1>LITERATURE CITED</h1>
<table>
<tbody>
<tr>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract" target="_blank"><img title="Abstract" border="0" alt="Abstract" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2" target="_blank"><img title="Material and Methods" border="0" alt="Material and Methods" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3" target="_blank"><img title="Results" border="0" alt="Results" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4" target="_blank"><img title="Discussion" border="0" alt="Discussion" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5" target="_blank"><img title="ACKNOWLEDGMENTS" border="0" alt="ACKNOWLEDGMENTS" src="http://www3.interscience.wiley.com/images/sec_up_small.gif"></a></td>
<td><a href="http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6" target="_blank"><img title="LITERATURE CITED" border="0" alt="LITERATURE CITED" src="http://www3.interscience.wiley.com/images/sec_here_small.gif"></a></td>
</tr></tbody></table>
<ul>
<li>
<p><a name="12a0b9da95851476_b1"> </a><span><span><span>Aron</span>, <span>S.</span></span>, <span><span>L. d.</span> <span>Menten</span></span>, <span><span>D. R. v.</span> <span>Bockstaele</span></span>, <span><span>S. M.</span> <span>Blank</span></span>,
<span><span>Y.</span> <span>Roisin</span></span><span></span></span>.
<span>2005</span>. <span>When hymenopteran males reinvented
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