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      Determining social and population structures requires multiple approaches: A case study of the desert ant Cataglyphis israelensis

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          Abstract

          The remarkable diversity of ant social organization is reflected in both their life history and population kin structure. Different species demonstrate a high variation with respect to both social structure and mating strategies: from the ancestral colony type that is composed of a single queen (monogyny), singly inseminated (monoandry), to the more derived states of colonies headed by a multiply inseminated queen (polyandry), to colonies composed of multiple queens (polygyny) that are either singly or multiply inseminated. Moreover, the population structure of an ant species can range from multicoloniality to polydomy to supercoloniality, and Cataglyphis is considered to be a model genus in regard to such diversity. The present study sought to determine the social and population structure of the recently described C. israelensis species in Israel. For this purpose we employed a multidisciplinary approach, rather than the commonly used single approach that is mostly based on genetics. Our study encompassed behavior (nest insularity/openness), chemistry (composition of nestmate recognition signals and cuticular hydrocarbons), and genetics (microsatellite polymorphism). Each approach has been shown to possess both advantages and disadvantages, depending on the studied species. Our findings reveal that C. israelensis colonies are headed by a single, multiply inseminated queen and that the population structure is polydomous, with each colony comprising one main nest and several additional satellite nests. Moreover, our findings demonstrate that none of the above‐noted approaches, when employed individually, is suitable or sufficient in itself for delineating population structure, thus emphasizing the importance of using multiple approaches when assessing such complex systems.

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          Most cited references41

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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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            COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients.

            The software package COANCESTRY implements seven relatedness estimators and three inbreeding estimators to estimate relatedness and inbreeding coefficients from multilocus genotype data. Two likelihood estimators that allow for inbred individuals and account for genotyping errors are for the first time included in this user-friendly program for PCs running Windows operating system. A simulation module is built in the program to simulate multilocus genotype data of individuals with a predefined relationship, and to compare the estimators and the simulated relatedness values to facilitate the selection of the best estimator in a particular situation. Bootstrapping and permutations are used to obtain the 95% confidence intervals of each relatedness or inbreeding estimate, and to test the difference in averages between groups. © 2010 Blackwell Publishing Ltd.
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              Lifetime monogamy and the evolution of eusociality.

              All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton's rule (br(s) > r(o)c), but implies that relatedness cancels out of the equation because average relatedness to siblings (r(s)) and offspring (r(o)) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton's rule.
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                Author and article information

                Contributors
                talireiner@gmail.com
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                10 December 2018
                December 2018
                : 8
                : 24 ( doiID: 10.1002/ece3.2018.8.issue-24 )
                : 12365-12374
                Affiliations
                [ 1 ] School of Zoology, George S. Wise Faculty of Life Sciences Tel Aviv University Tel Aviv Israel
                Author notes
                [*] [* ] Correspondence

                Tali Reiner Brodetzki, School of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel.

                Email: talireiner@ 123456gmail.com

                Author information
                http://orcid.org/0000-0002-1705-2056
                http://orcid.org/0000-0001-9678-9429
                Article
                ECE34535
                10.1002/ece3.4535
                6308896
                0e40a009-db41-42ef-9096-e0729b05149c
                © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 14 February 2018
                : 08 August 2018
                : 15 August 2018
                Page count
                Figures: 3, Tables: 1, Pages: 10, Words: 14636
                Funding
                Funded by: Israel Science Foundation
                Award ID: 844/13
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece34535
                December 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.5.4 mode:remove_FC converted:28.12.2018

                Evolutionary Biology
                cuticular hydrocarbons,microsatellite analysis,polydomy
                Evolutionary Biology
                cuticular hydrocarbons, microsatellite analysis, polydomy

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