Characterization of a New Set of Microsatellite Markers Suggests Polygyny and Polyandry in Atta cephalotes (Hymenoptera: Formicidae)

The leaf-cutting ant, Atta cephalotes L. (1758), is a major herbivore with great economic impact in the Neotropics. Because of its broad range and human-mediated dissemination, the ecology of this ant has received considerable attention; however, questions concerning its population genetics, dispersal, and social structure remain unexplored. Here, we aimed to identify and provide information on molecular and statistical performance of a suite of polymorphic microsatellite markers for A. cephalotes while demonstrating their utility for further genetic studies. We designed primer sequences targeting thousands of microsatellite loci and then screened 30 of these for amplification and polymorphism. Fifteen of these loci were selected and used to evaluate their polymorphism using 74 ants sampled from 15 different nests of the same location. This set of 15 loci exhibited variation of 2–20 alleles, with a mean heterozygosity of 0.57. All loci followed Hardy–Weinberg expectations with no evidence of linkage disequilibrium, while two loci showed evidence of null alleles. Our preliminary analysis suggested substantial nest differentiation with no population viscosity within the sampled location, as well as colonies with multiple queens (polygyny) and paternity (polyandry). Our newly identified microsatellites have proven to be highly informative to investigate gene flow, social structure and reproduction of this key agricultural pest.

Imperfect strategy transmission can reverse the role of population viscosity on the evolution of altruism

Population viscosity, i.e., low emigration out of the natal deme, leads to high within-deme relatedness, which is beneficial to the evolution of altruistic behavior when social interactions take place among deme-mates. However, a detrimental side-effect of low emigration is the increase in competition among related individuals. The evolution of altruism depends on the balance between these opposite effects. This balance is already known to be affected by details of the life cycle; we show here that it further depends on the fidelity of strategy transmission from parents to their offspring. We consider different life cycles and identify thresholds of parent-offspring strategy transmission inaccuracy, above which higher emigration can increase the frequency of altruists maintained in the population. Predictions were first obtained analytically assuming weak selection and equal deme sizes, then confirmed with stochastic simulations relaxing these assumptions. Contrary to what happens with perfect strategy transmission from parent to off-spring, our results show that higher emigration can be favorable to the evolution of altruism.

Kin-dependent dispersal influences relatedness and genetic structuring in a lek system

Kin selection and dispersal play a critical role in the evolution of cooperative breeding systems. Limited dispersal dramatically increases relatedness in spatially structured populations (population viscosity), with the result that neighbours tend to be genealogical relatives. Yet the increase in neighbours’ performance through altruistic interaction may also result in habitat saturation and thus exacerbate local competition between kin. Our goal was to detect the footprint of kin selection and competition by examining the spatial structure of relatedness and by comparing non-effective and effective dispersal in a population of a lekking bird, Tetrao urogallus. For this purpose, we analysed capture–recapture and genetic data collected over a 6-year period on a spatially structured population of T. urogallus in France. Our findings revealed a strong spatial structure of relatedness in males. They also indicated that the population viscosity allowed male cooperation through two non-exclusive mechanisms. First, at their first lek attendance, males aggregate in a lek composed of relatives. Second, the distance corresponding to non-effective dispersal dramatically outweighed effective dispersal distance, which suggests that dispersers incur high post-settlement costs. These two mechanisms result in strong population genetic structuring in males. In females, our findings revealed a lower level of spatial structure of relatedness and genetic structure in respect to males. Additionally, non-effective dispersal and effective dispersal distances in females were highly similar, which suggests limited post-settlement costs. These results indicate that kin-dependent dispersal decisions and costs are factors driving the evolution of cooperative courtship and have a genetic footprint in wild populations.

Population viscosity suppresses disease emergence by preserving local herd immunity

Animal reservoirs for infectious diseases pose ongoing risks to human populations. In this theory of zoonoses, the introduction event that starts an epidemic is assumed to be independent of all preceding events. However, introductions are often concentrated in communities that bridge the ecological interfaces between reservoirs and the general population. In this paper, we explore how the risks of disease emergence are altered by the aggregation of introduction events within bridge communities. In viscous bridge communities, repeated introductions can elevate the local prevalence of immunity. This local herd immunity can form a barrier reducing the opportunities for disease emergence. In some situations, reducing exposure rates counterintuitively increases the emergence hazards because of off-setting reductions in local immunity. Increases in population mixing can also increase emergence hazards, even when average contact rates are conserved. Our theory of bridge communities may help guide prevention and explain historical emergence events, where disruption of stable economic, political or demographic processes reduced population viscosity at ecological interfaces.

The sociobiology of sex: inclusive fitness consequences of inter-sexual interactions

The diversity of social interactions between sexual partners has long captivated biologists, and its evolution has been interpreted largely in terms of ‘direct fitness’ pay-offs to partners and their descendants. Inter-sexual interactions also have ‘indirect effects’ by affecting the fitness of relatives, with important consequences for inclusive fitness. However, inclusive fitness arguments have received limited consideration in this context, and definitions of ‘direct’ and ‘indirect’ fitness effects in this field are often inconsistent with those of inclusive fitness theory. Here, we use a sociobiology approach based on inclusive fitness theory to distinguish between direct and indirect fitness effects. We first consider direct effects: we review how competition leads to sexual conflict, and discuss the conditions under which repression of competition fosters sexual mutualism. We then clarify indirect effects, and show that greenbeard effects, kin recognition and population viscosity can all lead to episodes of indirect selection on sexual interactions creating potential for sexual altruism and spite. We argue that the integration of direct and indirect fitness effects within a sociobiology approach enables us to consider a more diverse spectrum of evolutionary outcomes of sexual interactions, and may help resolving current debates over sexual selection and sexual conflict.

The evolution of cooperative breeding in birds: kinship, dispersal and life history

The evolution of cooperation among animals has posed a major problem for evolutionary biologists, and despite decades of research into avian cooperative breeding systems, many questions about the evolution of their societies remain unresolved. A review of the kin structure of avian societies shows that a large majority live in kin-based groups. This is consistent with the proposed evolutionary routes to cooperative breeding via delayed dispersal leading to family formation, or limited dispersal leading to kin neighbourhoods. Hypotheses proposed to explain the evolution of cooperative breeding systems have focused on the role of population viscosity, induced by ecological/demographic constraints or benefits of philopatry, in generating this kin structure. However, comparative analyses have failed to generate robust predictions about the nature of those constraints, nor differentiated between the viscosity of social and non-social populations, except at a coarse level. I consider deficiencies in our understanding of how avian dispersal strategies differ between social and non-social species, and suggest that research has focused too narrowly on population viscosity and that a broader perspective that encompasses life history and demographic processes may provide fresh insights into the evolution of avian societies.