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      Colony size is linked to paternity frequency and paternity skew in yellowjacket wasps and hornets

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          Abstract

          Background

          The puzzle of the selective benefits of multiple mating and multiple paternity in social insects has been a major focus of research in evolutionary biology. We examine paternity in a clade of social insects, the vespine wasps (the yellowjackets and hornets), which contains species with high multiple paternity as well as species with single paternity. This group is particularly useful for comparative analyses given the wide interspecific variation in paternity traits despite similar sociobiology and ecology of the species in the genera Vespula, Dolichovespula and Vespa. We describe the paternity of 5 species of yellowjackets ( Vespula spp.) and we perform a phylogenetically controlled comparative analysis of relatedness, paternity frequency, paternity skew, colony size, and nest site across 22 vespine taxa.

          Results

          We found moderate multiple paternity in four small-colony Vespula rufa-group species (effective paternity 1.5 – 2.1), and higher multiple paternity in the large-colony Vespula flavopilosa (effective paternity ~3.1). Our comparative analysis shows that colony size, but not nest site, predicts average intracolony relatedness. Underlying this pattern, we found that greater colony size is associated with both higher paternity frequency and reduced paternity skew.

          Conclusions

          Our results support hypotheses focusing on the enhancement of genetic diversity in species with large colonies, and run counter to the hypothesis that multiple paternity is adaptively maintained due to sperm limitation associated with large colonies. We confirm the patterns observed in taxonomically widespread analyses by comparing closely related species of wasps with similar ecology, behavior and social organization. The vespine wasps may be a useful group for experimental investigation of the benefits of multiple paternity in the future.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12862-014-0277-x) contains supplementary material, which is available to authorized users.

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          Most cited references94

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          COLONY: a program for parentage and sibship inference from multilocus genotype data.

          Pedigrees, depicting genealogical relationships between individuals, are important in several research areas. Molecular markers allow inference of pedigrees in wild species where relationship information is impossible to collect by observation. Marker data are analysed statistically using methods based on Mendelian inheritance rules. There are numerous computer programs available to conduct pedigree analysis, but most software is inflexible, both in terms of assumptions and data requirements. Most methods only accommodate monogamous diploid species using codominant markers without genotyping error. In addition, most commonly used methods use pairwise comparisons rather than a full-pedigree likelihood approach, which considers the likelihood of the entire pedigree structure and allows the simultaneous inference of parentage and sibship. Here, we describe colony, a computer program implementing full-pedigree likelihood methods to simultaneously infer sibship and parentage among individuals using multilocus genotype data. colony can be used for both diploid and haplodiploid species; it can use dominant and codominant markers, and can accommodate, and estimate, genotyping error at each locus. In addition, colony can carry out these inferences for both monoecious and dioecious species. The program is available as a Microsoft Windows version, which includes a graphical user interface, and a Macintosh version, which uses an R-based interface. © 2009 Blackwell Publishing Ltd.
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            Phylogenetic signal and linear regression on species data

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              Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach.

              Rates of molecular evolution vary widely between lineages, but quantification of how rates change has proven difficult. Recently proposed estimation procedures have mainly adopted highly parametric approaches that model rate evolution explicitly. In this study, a semiparametric smoothing method is developed using penalized likelihood. A saturated model in which every lineage has a separate rate is combined with a roughness penalty that discourages rates from varying too much across a phylogeny. A data-driven cross-validation criterion is then used to determine an optimal level of smoothing. This criterion is based on an estimate of the average prediction error associated with pruning lineages from the tree. The methods are applied to three data sets of six genes across a sample of land plants. Optimally smoothed estimates of absolute rates entailed 2- to 10-fold variation across lineages.
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                Author and article information

                Contributors
                kjl75@cornell.edu
                cc747@cornell.edu
                mikejuhl@comcast.net
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                30 December 2014
                30 December 2014
                2014
                : 14
                : 1
                : 2625
                Affiliations
                [ ]Department of Neurobiology and Behavior, Cornell University, Ithaca, NY USA
                [ ]Bee Man Exterminators LLC, Olympia, WA USA
                Article
                277
                10.1186/s12862-014-0277-x
                4298054
                25547876
                db9406b0-ade6-49c5-b4be-602fe9436267
                © Loope et al.; licensee BioMed Central. 2014

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 29 June 2014
                : 18 December 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Evolutionary Biology
                social insects,polyandry,multiple paternity,paternity skew,vespula,dolichovespula,vespa,social evolution

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