[Pollinator] Fwd: CONSERVATION GENETICS OF NEOTROPICAL POLLINATORS REVISITED: MICROSATELLITE ANALYSIS SUGGESTS THAT DIPLOID MALES ARE RARE IN ORCHID BEES
Peter Bernhardt
bernhap2 at slu.edu
Mon Jul 26 06:14:39 PDT 2010
---------- Forwarded message ----------
From: Neal Smith <smithn at stri.org>
Date: Sun, Jul 25, 2010 at 4:57 PM
Subject: CONSERVATION GENETICS OF NEOTROPICAL POLLINATORS REVISITED:
MICROSATELLITE ANALYSIS SUGGESTS THAT DIPLOID MALES ARE RARE IN ORCHID BEES
To: Neal Smith <smithn at si.edu>
*SCIENCE SENDINGS!!*
**
*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.........*
Evolution <http://www3.interscience.wiley.com/journal/117958524/home>
>
CONSERVATION GENETICS OF NEOTROPICAL POLLINATORS REVISITED: MICROSATELLITE
ANALYSIS SUGGESTS THAT DIPLOID MALES ARE RARE IN ORCHID BEES
Rogério O. Souza 1,2 , Marco A. Del Lama 1 , Marcelo Cervini 3 , Norma
Mortari 3 , Thomas Eltz 4 , Yvonne Zimmermann 4 , Carola Bach 4 , Berry J.
Brosi 5,6 , Sevan Suni 7 , J. Javier G. Quezada-Euán 8 , and Robert J.
Paxton 9,10,11,12
1 Laboratório de Genética Evolutiva de Himenópteros, Departamento de
Genética e Evolução, Universidade Federal de São Carlos, CEP 13565-905, São
Carlos, São Paulo, Brazil 3 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 4 Sensory Ecology
Group, University of Düsseldorf, Universitätsstrasse 1, D-40225 Düsseldorf,
Germany 5 Department of Biology, Stanford University, 385 Serra Mall,
Stanford, California 94305 7 Center for Insect Science, University of
Arizona, Tucson, Arizona 85721 8 Departamento de Apicultura, Universidad
Autonoma de Yucatán, Mérida, Mexico 9 School of Biological Sciences,
Queen's University Belfast, 97 Lisburn Road, Belfast BT9 7BL, United Kingdom
12 E-mail: rjp246 at cornell.edu
Associate Editor: C. Jiggins
2 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.
6 Department of Environmental Studies, Emory University, Math & Science
Center, Suite E510, 400 Dowman Drive, Atlanta, Georgia 3032.
10 Department of Entomology, Cornell University, Comstock Hall, Ithaca, New
York 14853.
11 Institute for Biology, Martin-Luther-University Halle-Wittenberg, Hoher
Weg 8, D-06099 Halle (Saale), Germany.
Copyright (c) 2010, Society for the Study of Evolution
KEYWORDS
Complementary sex determination * csd * Euglossini * Hymenoptera
ABSTRACT
[image: Abstract] [image: Material and
Methods]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2>
[image:
Results]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3>
[image:
Discussion]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4>
[image:
ACKNOWLEDGMENTS]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5>
[image:
LITERATURE CITED]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6>
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.
------------------------------
Received November 16, 2009
Accepted May 31, 2010
DIGITAL OBJECT IDENTIFIER (DOI)
10.1111/j.1558-5646.2010.01052.x About
DOI<http://www3.interscience.wiley.com/doiinfo.html>
Article Text
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 (van Wilgenburg et al.
2006<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b59>;
but see Cowan and Stahlhut
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b14>;
de Boer et al. 2007,
2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b16>;
Heimpel and de Boer
2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b28>;
Verhulst et al.
2010<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b60>).
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 (Cook
1993<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b11>;
Cook and Crozier
1995<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b12>;
van Wilgenburg et al.
2006<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b59>).
slCSD may itself lead to lower effective population size (Ne) compared to
diploidy (Zayed
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b62>
).
All bees appear to be slCSD haplodiploids (van Wilgenburg et al.
2006<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b59>;
Zayed 2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b63>)
and there is growing evidence for decline in many groups (Brown and Paxton
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b6>;
Potts et al. 2010<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b44>);
unequivocal evidence is seen in solitary bees in England and the Netherlands
(Biesmeijer et al.
2006<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b3>),
bumblebees in Ireland (Fitzpatrick et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b24>),
and honey bees (Apis mellifera) in the USA (Oldroyd
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b36>;
vanEngelsdorp et al.
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b57>).
This is cause for concern because bees are important pollinators in natural
and agro-ecosystems (Klein et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b31>).
Pollination is an important ecosystem service that is being degraded by
anthropogenic changes (Kremen et al.
2002<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b32>;
Steffan-Dewenter et al.
2005<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b53>),
including habitat destruction, pollution, and facilitation of invasive
species (Mooney et al.
2005<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b35>).
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 (Zayed et al.
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65>).
Zayed and Packer's
(2005)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b64>theoretical
modeling concluded that diploid males exert a high genetic load
on populations, which could potentially drive a genetic extinction vortex in
slCSD haplodiploids.
The Euglossini comprise ca. 200 species of Neotropical bees that are the
sole pollinators of around 700 orchid species (Dressler
1982<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b19>;
Cameron 2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b7>;
Roubik and Hanson
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b48>).
Males collect perfumes from orchid blossoms and other sources in their hind
tibiae and later release them at mating sites, possibly to attract
females (Eltz
et al. 2005, 2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b21>).
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 (Roubik et al.
1996<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49>).
In contrast, Takahashi et al.
(2001)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55>found
very low (mean 0-2% per species) frequencies of 2N males in 14
Brazilian species. Zayed et al.
(2004)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65>subsequently
detected 13-56% (across populations) of Panamanian Euglossa
imperialis males to be diploid and inferred extremely limited gene flow and
low Ne in the species, supporting Roubik et al.'s
(1996)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49>view
that orchid bees exhibited low diversity at the sex locus. More
recently, López-Uribe et al.
(2007)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b33>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 (n= 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.
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., Brosi
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b5>)
whereas both sexes are thought to be extremely mobile (Janzen 1971,
1981<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b29>;
Dressler 1982<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b19>;
Cameron 2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b7>;
Dick et al. 2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b17>).
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 Eg.
imperialis from Panama, to reveal extremely low (0.5%) frequencies of 2N
males and very weak population genetic structure even across 500 km.
Material and Methods [image:
Abstract]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract>
[image:
Material and Methods]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2>
[image:
Results]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3>
[image:
Discussion]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4>
[image:
ACKNOWLEDGMENTS]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5>
[image:
LITERATURE CITED]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6>
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 (Table
1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1>,
Fig. 1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#f1>).
These included 143 males already genotyped using allozymes and
reported by Takahashi
et al. (2001)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55>.
In Panama, 257 males from three species were collected at odor baits; Eg.
imperialis was collected from three sites across March-May 2005, Eg.
tridentata from two sites across 16 days in March-April 2006 (both at
1,8-cineole baits) and Euglossa hemichlora from one site in September 2007
(at p-dimethoxybenzene baits, Fig.
1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#f1>).
In Mexico, 73 Euglossa aff. viridissima males (the lineage with three
mandibular teeth, 3D, to be described as a new species; Eltz et al. unpubl.
ms) and 57 Eg. viridissima males (the lineage with two mandibular teeth, 2D;
see Eltz et al.
2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b23>)
were collected at odor baits (p-dimethoxybenzene) from one site in March
2006 and May 2007. Finally, in Costa Rica, 140 Eulaema bombiformis 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 Brosi
(2009)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b5>.
Insects were stored in ethanol at -20°C or were dried and stored at room
temperature.
Table 1. Species name, collection site, number of males sampled
(nmales), number of polymorphic loci used (
n loci), range of expected intralocus allelic diversity (Hina, adjusted for
putative null alleles; see Tables S1 and S2), mean allelic diversity across
loci (Hexp, adjusted for putative null alleles), probability of detecting a
heterozygous male if diploid (Phet), 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 Figure
1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#f1>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.
------------------------------
Species Collection Site n males n loci H ina H exp P het 2N males 95% CIs
of 2N frequency Euglossa annectans São Carlos - SP, Brazil 17* 6 0.17-0.75
0.48 0.988 1* 0.002-0.288 Eg. chalybeata Manaus - AM, Brazil 19 6 0.28-0.72
0.60 0.998 0 Eg. cognata Villavicencio, Colombia 1 92 0 Eg.
cordata Caraguatatuba
- SP, Brazil 37* 8 0.30-0.88 0.63 >0.999 0 São Carlos - SP, Brazil
30* Eg.
fimbriata São Carlos - SP, Brazil 7* 8 0.25-0.86 0.56 >0.999 0 Eg.
hemichlora Santa Rita, Panama 43 3 0.62-0.84 0.75 0.987 0 Manaus - AM,
Brazil 30 6 0.44-0.81 0.67 >0.999 0 Eg. imperialis Barro Colorado, Panama
47 0 Fort Clayton, Panama 23 5 0.02-0.83 0.45 0.983 0 Gigante
Peninsula, Panama 28 Eg. intersecta Manaus - AM, Brazil 1 62 0 Eg.
mandibularis Viçosa - MG, Brazil 95*1 8 0.08-0.87 0.56 >0.999 1* 0-0.057 Eg.
melanotricha Analândia - SP, Brazil 8* 9 0.38-0.88 0.66 >0.999 0 Eg.
mixta Villavicencio, Colombia 3 5 0.44-0.67 0.49 0.968 0 Eg. moure Manaus -
AM, Brazil 1 72 0 Eg. pleosticta São Carlos - SP, Brazil 4* 9
0.38-0.75 0.63 >0.999 0 Camburí- SP, Brazil 2 Eg.
securigera Rifaina
- SP, Brazil 3 9 0.22-0.78 0.57 >0.999 0 São Carlos - SP, Brazil 3*
Eg. townsendi Araras - SP, Brazil 3 8 0.38-0.75 0.56 0.999 0 Rifaina
- SP, Brazil 1 Eg. tridentata Barro Colorado, Panama 60 2
0.67-0.89 0.78 0.964 1 0-0.049 Parque Natur. Metro., Panama 56
Eg.
truncata São Carlos - SP, Brazil 10* 7 0.42-0.78 0.65 >0.999 0 Eg.
viridis Villavicencio,
Colombia 1 92 0 Eg. aff viridissima 3D3 Xmatkuil, Mexico 73 2
0.85-0.89 0.87 0.984 0 Eg. viridissima 2D4 Xmatkuil, Mexico 57 2 0.59-0.87
0.73 0.948 0 Eulaema Manaus - AM, Brazil 21 11 0.58-0.89 0.79 >0.999 0
bombiformis Las Cruces, Costa Rica 140 9 0.16-0.61 0.34 0.981 2 0-0.051 El.
cingulata Manaus - AM, Brazil 8 7 0.47-0.81 0.63 >0.999 0 El. meriana Manaus
- AM, Brazil 26 10 0.27-0.89 0.69 >0.999 0 Cuiabá- MT, Brazil 4 Manaus
- AM, Brazil 4 Marliéria - ES, Brazil 5 Mimoso - MG,
Brazil 4 El. nigrita Poconé- MT, Brazil 3* 11 0.61-0.91 0.77
>0.999 0 Rifaina - SP, Brazil 5 S. J. Campos - SP, Brazil 5
São Carlos - SP, Brazil 5* Viçosa - MG, Brazil 5 Eufriesea
violacea São Carlos - SP, Brazil 16 10 0.37-0.85 0.59 >0.999 0 Viçosa -
MG, Brazil 37 Exaerete frontalis João Pessoa - PB, Brazil 8 3 0.66-0.78
0.74 0.983 0 Ex. smaragdina João Pessoa - PB, Brazil 50 3 0.79-0.83 0.81
0.993 0 São Carlos - SP, Brazil 1 Grand Total 1010 0.02-
0.91 0.62 0.991 5 0.002-0.010
------------------------------
*The same samples as analyzed by Takahashi et al.
(2001)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55>
; 1 n=76 new samples added in addition to those of Takahashi et al.
(2001)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55>
; 2For n=1 male analyzed, n loci=number of loci employed (see Table S1); 3All
males from the species with three mandibular teeth, 3D (see Eltz et
al. 2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b23>),
to be described as a new species (Eltz et al. unpubl. data). 4All males from
the species with two mandibular teeth, 2D (see Eltz et al.
2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b23>
).
------------------------------
Figure 1. Map of the Neotropics with the 22 sampling sites highlighted as
dots (five adjacent localities in Panama are given one dot).
[Normal View ]
DNA was extracted from legs or thoraxes using a high salt protocol (Paxton
et al. 1996<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b40>)
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 Euglossa cordata, Eulaema nigrita (Souza et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b52>),
and Euglossa annectans (Paxton et al.
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b42>);
these are unlinked loci that are in Hardy-Weinberg equilibrium (HWE) in the
species for which they were developed (Souza et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b52>;
Paxton et al. 2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b42>).
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 Paxton et al.
1996<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b68>).
Allele calling across these duplicate analyses of the same individual-locus
combination was identical. We therefore estimate extremely low genotyping
error rates.
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, Phet, as where
summation is across the N alleles at a locus and multiplication is
across Lloci. This assumes HWE, although moderate levels of inbreeding
have only a
slight effect on Phet (e.g., see Paxton et al.
2000<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b41>).
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 (Eg. annectans in Paxton et al.
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b42>;
Eg. cordata and El. nigrita in Souza et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b52>;
and Eg. viridissima in Zimmermann et al.
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b67>),
suggesting random mating in orchid bees.
Null alleles can nevertheless cause difficulties in microsatellite allele
scoring and lead to an overestimation of Phet. 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 (Hina) and Phet 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, n > 20 females for
5 species. Their genotypes were tested for the presence of null alleles
using MICRO-CHECKER (van Oosterhout et al.
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b58>)
and we reduced allelic diversity (Hina or expected heterozygosity accounting
for null alleles) and Phet for the three loci showing evidence of null
alleles using equation (4) of
Brookfield<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b4>(1996;
see Table S2). For the other loci, we calculated expected allelic
diversity (Hina or expected heterozygosity) from female genotypes using
GENEPOP (Raymond and Rousset
1995<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b45>).
We conservatively used the lowest estimates of Hina and Phet 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 (
http://statpages.org/confint.html).
Four species were collected at two or more sites spanning 4-538 km: Eg.
cordata (two sites), Eg. imperialis (three sites), Eg. tridentata (two
sites), and Eufriesea violacea (two sites; see Table
2<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2>)
and genotyped in the same laboratory. For each population pair, we computed
estimates of genetic differentiation to infer population connectivity. Both
FST and Hedrick's
(2005)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b26>unbiased
estimator of population differentiation,
GST', were calculated with MSA version 4.05 (Dieringer and Schlötterer
2003<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b18>)
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.
Table 2. Geographic distances between pairs of populations of orchid bees
(males) and genetic differentiation measured as FST and Hedrick's
(2005)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b26>
GST', with exact P values (1000 permutations) from MSA (Dieringer and
Schlötterer 2003<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b18>).
For locations, see Figure
1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#f1>
.
------------------------------
Pair of populations n (males) n (loci) Distance (km) FST (P) G ST'
(P) Euglossa
cordata (Brazil) 37 8 310 0.024 (0.005) 0.175 (0.037) Caraguatatuba versus
São Carlos 30 Euglossa imperialis (Panama) 47 5 34 0.012
(0.176) 0.014
(0.827) Barro Colorado versus Fort Clayton 23 Euglossa
imperialis(Panama)
47 5 4 -0.011 (0.767) 0.096 (0.422) Barro Colorado versus Gigante Penninsula
28 Euglossa imperialis (Panama) 23 5 32 0.004 (0.308) 0.038
(0.710) Fort Clayton versus Gigante Penninsula 28 Euglossa
tridentata (Panama) 60 2 36 0.001 (0.354) 0.072 (0.379) Barro Colorado
versus Parque Natural Metropolitano 56 Eufriesea violacea (Brazil)
16 10 538 -0.025 (0.991) 0.074 (0.598) São Carlos versus Viçosa 37
------------------------------
Results [image:
Abstract]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract>
[image:
Material and Methods]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2>
[image:
Results]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3>
[image:
Discussion]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4>
[image:
ACKNOWLEDGMENTS]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5>
[image:
LITERATURE CITED]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6>
Allelic diversity accounting for null alleles (expected heterozygosity) of
our loci, Hina, ranged from 0.02 to 0.96 (Table
1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1>).
It was generally above 0.5 for most loci in most species (Tables S1 and S2)
and averaged 0.62 (Table
1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1>).
Hina differed little between males and females; it was greater by 0.044 in
males versus females (n= 5 species and n= 26 locus-species combinations),
suggesting that our estimates of Phet in species for which we did not sample
females are only slightly inflated. Using 2-11 loci per species gave an
average Phet 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.
We detected five heterozygotes among the 1010 males that we genotyped, one
each in Eg. annectans, Eg. mandibularis, and Eg. tridentata, and two in El.
bombiformis (Table
1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1>).
The Eg. mandibularis male heterozygous at microsatellite locus Egc24 (Table
S1) was the same individual that Takahashi et al.
(2001)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55>also
detected by allozyme analysis as a heterozygote. We additionally
detected one heterozygous Eg. annectans male (heterozygous at loci Egc18 and
Egc24; see Table S1) that Takahashi et al.
(2001)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b55>found
to be homozygous by allozyme analysis. Over all males, and accounting
for genetic nondetection errors (i.e., where Phet < 1), diploid male
frequency averaged 0.005 (95% CI's 0.002-0.010).
Population differentiation in orchid bees was generally small and
nonsignificant (Table
2<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2>),
suggesting considerable gene flow. For the Eg. imperialis dataset comprising
three Panamanian populations 4-34 km apart, global FST= 0.001 (P= 0.384) and
GST'= 0.034 (P= 0.786). Pairwise measures of Eg. imperialis population
differentiation were similarly not significantly different from zero (Table
2<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2>).
The two Eg. tridentata populations separated by 36 km were also not
significantly differentiated (Table
2<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2>).
The two Eg. cordata populations separated by 310 km showed low, though
significant, estimates of FST and GST' (Table
2<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2>).
In contrast, the two Ef. violacea populations separated by 538 km were not
significantly differentiated (Table
2<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t2>),
suggesting considerable gene flow between them.
Discussion [image:
Abstract]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract>
[image:
Material and Methods]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2>
[image:
Results]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3>
[image:
Discussion]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4>
[image:
ACKNOWLEDGMENTS]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5>
[image:
LITERATURE CITED]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6>
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 (Dick et al.
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b17>),
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 Ne, and that
they do not suffer from inbreeding through genetic drift and loss of
csddiversity.
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 Ne (Roubik et al.
1996<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49>;
Zayed et al. 2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65>;
López-Uribe et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b33>)?
We offer two explanations.
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 Roubik et al.
(1996)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49>that
exhibited high 2N male frequencies (Roubik
et al. 1996<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49>,
their Table 1<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#t1>),
and we included two species (Eg. imperialis and Eg. tridentata) from the
same sampling sites as Roubik et al.
(1996)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49>.
Furthermore, we did not detect any 2N males among the 98 Eg.
imperialismales that we analyzed (95% CI's 0-3.8%) from the same three
sampling sites
at which Zayed et al.
(2004)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65>found
37.7% of Eg.
imperialis 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 Roubik et
al. (1996)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b49>and
Zayed
et al. (2004)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65>sampled
but we did not.
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 (Schlötterer
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b50>).
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 (Eg.
annectans in Paxton et al.
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b42>;
Eg. cordata and El. nigrita in Souza et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b52>;
Euglossa igniventris, T. Eltz, unpubl. data; EG. hemichlora, Eg. townsendi, Eg.
viridissima, and Exaerete smaragdina 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 (Eltz et al.
1998<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b20>)
or genome size estimation by flow cytometry (Aron et al.
2005<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b1>;
Cournault and Aron
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b13>),
are needed to support our microsatellite-based conclusions.
Our interpretation of orchid bee population genetics, that they have low 2N
male production, very weak population structure, high gene flow, and high Ne,
fits with many independent observations of the taxon. First, individual
orchid bees have been reported to travel long distances (>20 km;
Janzen 1971<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b29>).
Second, other orchid bee species are common faunal elements in natural and
disturbed habitats (Brosi
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b5>)
and even in urban centers (López-Uribe et al.
2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b34>).
Third, census data suggest that orchid bee abundance and diversity appear to
have been maintained (Roubik
2001<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b47>),
even within the highly fragmented Atlantic rainforest of Brazil (Tonhasca et
al. 2002<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b56>).
Finally, results from the phylogeographic study of Dick et al.
(2004)<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b17>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.
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 (Zayed et
al. 2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65>)
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 (Paxton et al.
2000<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b41>).
Also, severely bottlenecked populations of the sweat bee Lasioglossum
leucozonium with high 2N male frequencies detected by microsatellite
genotyping have recently expanded across Eastern USA (Zayed et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b66>),
suggesting that high 2N male frequencies are not necessarily correlated with
population decline in this invasive species. Yet for the honey bee (A.
mellifera) with a well-characterized system of sex determination based on
slCSD (Beye et al.
2003<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b2>),
high frequencies of 2N males have a catastrophic effect on colony
survival (Woyke
1980<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b61>),
as in other social bees (Plowright and Pallett
1979<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b43>;
Carvalho 2001<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b8>)
and ants (Ross and Fletcher
1986<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b46>).
An appropriate test of the diploid male extinction vortex (Zayed and Packer
2005<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b64>)
and the idea that the frequency of 2N males is a sensitive measure of
pollinator decline (Zayed et al.
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b65>)
awaits analysis of slCSD populations at their range margins or of those that
have been anthropogenically compromised. Eusocial Hymenoptera such as
bumblebees (e.g., Takahashi et al.
2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b54>)
may be more suitable subjects for such a test than the largely solitary and
subsocial orchid bees (cf. Cocom Pech et al.
2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b10>)
because hymenopteran eusociality is associated with reduced genetic
diversity and low Ne (Pamilo et al. 1978,
1997<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b38>;
Graur 1985<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b25>;
Hedrick and Parker
1997<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b27>;
Chapman and Bourke
2001<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b9>;
Packer and Owen
2001<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b37>
).
Although bees are thought to possess slCSD (van Wilgenburg et al.
2006<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b59>),
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; de Boer et al.
2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b15>)
and diploid males in hymenopterans with regular inbreeding produce fertile
diploid males (de Boer et al.
2007<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b16>;
Cournault and Aron
2009<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b13>);
in one wasp with regular inbreeding, diploid males may even produce haploid
sperm (Cowan and Stahlhut
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b14>).
Sex determination through genomic imprinting has also been recently
demonstrated in the haplodiploid hymenopteran Nasonia (Verhulst et al.
2010<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b60>).
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.
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; Soares
et al. 2003<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b51>),
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 (Zayed and Packer
2005<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b64>),
possibly because of high gene flow maintaining adequate allelic diversity at
the sex locus. Second, they appear to be highly mobile, again
increasing Nebeyond 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 (Roubik and Hanson
2004<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b48>;
Eltz et al. 2008<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#b23>)
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.
Associate Editor: C. Jiggins
ACKNOWLEDGMENTS [image:
Abstract]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract>
[image:
Material and Methods]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2>
[image:
Results]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3>
[image:
Discussion]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4>
[image:
ACKNOWLEDGMENTS]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5>
[image:
LITERATURE CITED]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6>
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.
LITERATURE CITED [image:
Abstract]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#abstract>
[image:
Material and Methods]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss2>
[image:
Results]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss3>
[image:
Discussion]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss4>
[image:
ACKNOWLEDGMENTS]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss5>
[image:
LITERATURE CITED]<http://www3.interscience.wiley.com/cgi-bin/fulltext/123526445/main.html,ftx_abs#ss6>
-
Aron, S., L. d. Menten, D. R. v. Bockstaele, S. M. Blank, Y. Roisin.
2005. When hymenopteran males reinvented diploidy. Curr. Biol. 15:824-827.
Links<http://www3.interscience.wiley.com/cgi-bin/reflink?object=TYPE%3DJCIT%26BIBID%3D1%26SNM%3DAron%26SNM%3DMenten%26SNM%3DBockstaele%26SNM%3DBlank%26SNM%3DRoisin%26FNM%3DS.%26FNM%3DL.%20d.%26FNM%3DD.%20R.%20v.%26FNM%3DS.%20M.%26FNM%3DY.%26ATL%3DWhen%20hymenopteran%20males%20reinvented%20diploidy%26JTL%3DCurr.%20Biol.%26PYR%3D2005%26VID%3D15%26PPF%3D824%26ADOI%3D10.1111/j.1558-5646.2010.01052.x%26EVIEW%3DY%26ENABLEISI%3DN%26ENABLECAS%3DY%26ENABLEPM%3DY>
-
Beye, M., M. Hasselmann, M. K. Fondrk, R. E. Page, S. W. Omholt. 2003. The
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