On Some Genetic Consequences of Social Structure, Mating Systems, Dispersal, and Sampling
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On some genetic consequences of social structure, mating systems, dispersal, and sampling Bárbara R. Parreiraa,b,1 and Lounès Chikhia,c aInstituto Gulbenkian de Ciência, 2780-156 Oeiras, Portugal; bDepartamento de Biologia Vegetal, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisbon, Portugal; and cCNRS, Université Paul Sabatier, Ecole Nationale de Formation Agronomique, UMR5174 EDB (Laboratoire Évolution & Diversité Biologique), F-31062 Toulouse, France Edited by Mark G. Thomas, University College London, London, United Kingdom, and accepted by the Editorial Board May 13, 2015 (received for review August 7, 2014) Many species are spatially and socially organized, with complex 26). A mathematical theory was first formalized by Chesser (23, social organizations and dispersal patterns that are increasingly 24), who showed that the accumulation of genetic variation documented. Social species typically consist of small age-struc- within and among breeding groups can be predicted from mating tured units, where a limited number of individuals monopolize and dispersal strategies. This work demonstrated that breeding reproduction and exhibit complex mating strategies. Here, we groups may appear outbred despite high coancestry among the model social groups as age-structured units and investigate the group members. However, this and other seminal studies (22, genetic consequences of social structure under distinct mating 25–27) have been neglected and sometimes misinterpreted by strategies commonly found in mammals. Our results show that population geneticists and ecologists alike. For example, empirical sociality maximizes genotypic diversity, which contradicts the be- studies documenting outbreeding within social groups (SGs) have lief that social groups are necessarily subject to strong genetic drift interpreted it as a consequence of inbreeding avoidance or as and at high risk of inbreeding depression. Social structure gener- evidence for sex-biased migration. Although this is in agreement ates an excess of genotypic diversity. This is commonly observed in with Chesser’s study on female philopatry (23), it overlooked ecological studies but rarely reported in population genetic studies Chesser’s later results (24) showing that social structure can lead that ignore social structure. This heterozygosity excess, when to outbreeding even without sex-biased migration. detected, is often interpreted as a consequence of inbreeding Ecological data on relatedness and dispersal show that social avoidance mechanisms, but we show that it can occur even in species exhibit kin recognition and sex-biased dispersal. For ex- the absence of such mechanisms. Many seemly contradictory re- ample, active kin recognition has been described in many co- sults from ecology and population genetics can be reconciled by operatively breeding passerine species (28), and in mammalian genetic models that include the complexities of social species. We species, where SGs are generally composed of related females, find that such discrepancies can be explained by the intrinsic prop- males are usually the dispersing sex (1, 29). The amount of ge- erties of social groups and by the sampling strategies of real pop- netic data gathered from social species has also increased sig- ulations. In particular, the number of social groups and the nature nificantly over the last decades. Most genetic studies within of the individuals that compose samples (e.g., nonreproductive social units report a higher proportion of heterozygotes than and reproductive individuals) are key factors in generating out- expected under random mating [i.e., evidence for heterozygote breeding signatures. Sociality is an important component of pop- excess (outbreeding)]. This finding was described, for example, ulation structure that needs to be revisited by ecologists and in yellow-bellied and alpine marmots (30, 31), white-tailed deers population geneticists alike. (32), and in black-tailed prairie dogs (33). In comparison with the behavioral ecology studies that rec- sociality | social structure | mating system | genotypic diversity | ognize social units as the basic study unit, most population ge- inbreeding avoidance netic studies are carried out at the “population” level, where a “population” is frequently a conglomeration of SGs. The latter ociality is one of the most striking features in the Animal SKingdom. A large number of animal species, including hu- Significance mans, are social. Social systems have evolved in several distinct taxa, such as insects, birds, and mammals (1–4). Whereas some Many species live in socially structured populations, forming animals are highly social and live in groups for their entire life, cohesive units with kin structure. Yet, sociality has been others form groups only for a short period. The diversity of social neglected by population geneticists under the assumption that organizations ranges from eusociality in insects or communal social groups can be seen as small demes subjected to signifi- breeding in vertebrates to solitary life in some mammalian spe- cant genetic drift. Such demes are usually considered to be cies (5–9). Even among closely related species, this diversity can susceptible to inbreeding, with inbreeding avoidance becom- be wide (2, 10). For example, among the great apes, gorillas live ing a major force explaining dispersal strategies. We find that in single-male harem systems, whereas chimpanzees live in large social structure is highly effective in maintaining high geno- multimale/multifemale aggregations forming hierarchical com- typic and genetic diversity levels, without invoking sex-biased munities of related males with coalition strategies (11, 12), and dispersal or inbreeding avoidance mechanisms. These findings orangutans exhibit a semisolitary lifestyle where the territory of should change the way we perceive social groups. one male can include the territory of several related females (13). For decades, much of the theoretical work on sociality has fo- – Author contributions: B.R.P. and L.C. designed research; B.R.P. performed research; L.C. cused on its origins (14 18). It is generally thought that group-living contributed new reagents/analytic tools; B.R.P. and L.C. analyzed data; and B.R.P. and L.C. confers fitness benefits to individuals (19–21). This view has had a wrote the paper. profound impact on the interpretation of social behavior. Indeed, it The authors declare no conflict of interest. is still hotly debated whether these benefits are at the origin of This article is a PNAS Direct Submission. M.G.T. is a guest editor invited by the Editorial sociality, or if they are a side-effect of the existence of kin groups Board. with stable bonds that appeared for other reasons (6). 1To whom correspondence should be addressed. Email: [email protected]. Sociality has been discussed by population geneticists for This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. several decades, but mostly from a theoretical point of view (22– 1073/pnas.1414463112/-/DCSupplemental. E3318–E3326 | PNAS | Published online June 16, 2015 www.pnas.org/cgi/doi/10.1073/pnas.1414463112 Downloaded by guest on September 25, 2021 studies, including those on highly social species, often find no prising 50 SGs until equilibrium, and measured genetic diversity PNAS PLUS signature of deviation from random-mating, [i.e., the proportion and inbreeding using traditional population genetics statistics. of heterozygotes meets Hardy–Weinberg (HW) proportions, in- dicating neither outbreeding nor inbreeding (25)]; this is, for Population Structure, Social Structure, and the Partitioning of Genetic example, the case of orangutans (34) and sifakas (35), among Diversity. We found that the subdivision of populations into SGs others. As a consequence, population geneticists have tended to lead to a higher (11–63%) genetic diversity than predicted under ignore sociality as an important source of genetic structure or the WF framework (Fig. 2, Fig. S1, and Table S1). This finding have considered SGs simply as small random-mating units (36, suggests that classic population genetics models may in many 37). This approach corresponds to the classic Wright–Fisher cases underestimate the genetic diversity found in real species model (WF) framework in which SGs are isolated demes with and hence lead to biased estimates (e.g., lower effective sizes or small effective sizes. This view has wide-ranging consequences. mutation rates) when applied to social species. Moreover, indi- First, because of the small effective sizes it is expected that SGs vidual heterozygosity within SGs (observed heterozygosity) was should be at high risk of inbreeding depression (36, 38). Second, equal to the expected heterozygosity at the population level based on the fact that small demes are subject to high genetic (HT), suggesting that the social structure is maintaining indivi- drift, the Bush–Wilson theory (39, 40) postulates that the fixation dual diversity at the maximum possible level rather than reducing of chromosomal rearrangements should be frequent and pro- it (Fig. S2). Therefore, social structure appears to be highly ef- mote an acceleration of the evolution rate in social species. This ficient in maintaining diversity within individuals and within SGs. theory has been criticized by behavioral ecologists who observed Interestingly, we found that genetic diversity was always high, higher, rather than lower, levels of heterozygosity in