Abstract

Given the hybrid genomic constitutions and increased ploidy of many asexual animals, the identification of processes governing the origin and maintenance of clonal diversity provides useful information about the evolutionary consequences of interspecific hybridization, asexuality and polyploidy. In order to understand the processes driving observed diversity of biotypes and clones in the Cobitis taenia hybrid complex, we performed fine-scale genetic analysis of Central European hybrid zone between two sexual species using microsatellite genotyping and mtDNA sequencing. We found that the hybrid zone is populated by an assemblage of clonally (gynogenetically) reproducing di-, tri- and tetraploid hybrid lineages and that successful clones, which are able of spatial expansion, recruit from two ploidy levels, i.e. diploid and triploid. We further compared the distribution of observed estimates of clonal ages to theoretical distributions simulated under various assumptions and showed that new clones are most likely continuously recruited from ancestral populations. This suggests that the clonal diversity is maintained by dynamic equilibrium between origination and extinction of clonal lineages. On the other hand, an interclonal selection is implied by nonrandom spatial distribution of individual clones with respect to the coexisting sexual species. Importantly, there was no evidence for sexually reproducing hybrids or clonally reproducing non-hybrid forms. Together with previous successful laboratory synthesis of clonal Cobitis hybrids, our data thus provide the most compelling evidence that 1) the origin of asexuality is causally linked to interspecific hybridization; 2) successful establishment of clones is not restricted to one specific ploidy level and 3) the initiation of clonality and polyploidy may be dynamic and continuous in asexual complexes.

Highlights

  • In many animal and plant taxa sexual and parthenogenetic biotypes coexist, which makes them ideal models to test the validity of theoretical predictions about the evolution of sex

  • Sampling and Genotyping Scoring of allozyme loci and S7 sequence variability in cases where the distinction of genomes was problematic led to the identification of the following biotypes (Table S2, Figure 1c): (1) diploids with 38 individuals C. elongatoides, 66 of C. taenia, and 81 of ET hybrids; (2) triploid hybrids with some combinations of C. elongatoides, C. taenia, or C. tanaitica genome (55 EET, 54 ETT, 25 EEN, 62 ETN); and (3) tetraploid biotypes (12 EEET, 12 EEEN, 14 ETTN, and 1 EENN)

  • When we pooled all parental individuals into the species-specific datasets, we observed no deviations from HW in C. elongatoides, but in C. taenia the locus cota_006 showed a significant lack of heterozygotes, resulting in significantly positive FIS

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Summary

Introduction

In many animal and plant taxa sexual and parthenogenetic biotypes coexist (we refer to such systems as ‘‘asexual complexes’’), which makes them ideal models to test the validity of theoretical predictions about the evolution of sex. Because coexisting biotypes often comprise several ploidy levels, asexual complexes provide an excellent opportunity to study the consequences of polyploidisation. Detailed investigations into some model asexual complexes have served as test-cases for theoretical predictions, but have directly stimulated the formulation of other hypotheses about the evolution of asexuality and polyploidy. Corley and Moore [10] observed difficulties in switching to asexual reproduction in a complex of parthenogenetic cockroaches and argued that such difficulties may explain the dominance of sex in eukaryotes in general (an analogous hypothesis has subsequently been raised by [11] and most recently by Stock et al [8] under the name ‘‘rare formation hypothesis’’)

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