Detection of Cryptic Sex in Automictic Populations: Theoretical Expectations and a Case Study in Cataglyphis Desert Ants

Alexandre Kuhn,Olivier J Hardy,Serge Aron

doi:10.3389/fevo.2021.741959

Alexandre Kuhn, Olivier J Hardy + Show 1 more

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https://doi.org/10.3389/fevo.2021.741959

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Abstract

Reproductive strategies are diverse and a whole continuum of mixed systems lies between strict sexuality and strict clonality (apomixis), including automixis, a parthenogenetic mode of reproduction involving a meiosis and increasing homozygosity over generations. These various systems impact the genetic structure of populations, which can therefore be used to infer reproductive strategies in natural populations. Here, we first develop a mathematical model, validated by simulations, to predict heterozygosity and inbreeding in mixed sexual-automictic populations. It highlights the predominant role of the rate of heterozygosity loss experienced during automixis (γ), which is locus dependent. Whenγis low, mixed populations behave like purely sexual ones until sex becomes rare. In contrast, whenγis high, the erosion of genetic diversity is tightly correlated to the rate of sex, so that the individual inbreeding coefficient can inform on the ratio of sexual/asexual reproduction. In the second part of this study, we used our model to test the presence of cryptic sex in a hybridogeneticCataglyphisant where new queens are produced parthenogenetically, leaving males with an apparent null fitness while they are essential to colony development as sperm is required to produce workers. Occasional sexual production of queens could resolve this paradox by providing males some fertile progeny. To determine whether this occurs in natural populations, we simulated genotypic datasets in a population under various regimes of sexual vs. asexual reproduction for queen production and compared the distribution of inbreeding, expected heterozygosity and inter-individual relatedness coefficients with those observed in a natural population ofCataglyphis mauritanicausing microsatellites. Our simulations show that the distribution of inter-individual relatedness coefficients was particularly informative to assess the relative rate of sexual/asexual reproduction, and our dataset was compatible with pure parthenogenesis but also with up to 2% sexual reproduction. Our approach, implemented in an R script, should be useful to assess reproductive strategies in other biological models.

Highlights

Understanding how sexual or asexual reproduction affects the genetic structure and dynamics of populations is a major concern in evolutionary biology (Balloux et al, 2003; Halkett et al, 2005; Otto, 2009)
The relatedness between queens followed a bimodal distribution within each lineage: some pairs had very similar genotypes, presumably because they descended from a recent common ancestor under pure automixis, while other queens had divergent genotypes, presumably because they arose from intra-lineage sexual reproduction or because they accumulated many mutations since their last common ancestor (Kuhn et al, 2017)
In the first part of this study, we used both analytical approach and stochastic individual-based simulations to describe the dynamics of genetic diversity in mixed sexualautomictic populations

Summary

Introduction

Understanding how sexual or asexual reproduction affects the genetic structure and dynamics of populations is a major concern in evolutionary biology (Balloux et al, 2003; Halkett et al, 2005; Otto, 2009). In diploid organisms and for finite populations, models predict that sexual reproduction should maintain higher genotypic but lower allelic diversity than clonality (Balloux et al, 2003; Halkett et al, 2005) This is because recombination associated with sexual reproduction shuffles genes between individuals, while genomes are inherited as a block under strict asexual reproduction. In the last 15 years, a number of models have been developed to determine the consequences of such mixed systems on population genetic structure and to estimate the rate of clonal vs sexual reproduction in natural populations (e.g., Balloux et al, 2003; Bengtsson, 2003; Ali et al, 2016; Reichel et al, 2016) These models usually consider how varying degrees of sexual reproduction affect the genetic structure of populations characterized by asexual reproduction through apomictic parthenogenesis (i.e., parthenogenetic reproduction without recombination, similar to mitosis). An important fraction (especially in animals) of parthenogenetically reproducing organisms do so through automixis, an asexual but non-clonal mode of reproduction (Mogie, 1986; Stenberg and Saura, 2009; Engelstädter, 2017)

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