General environmental heterogeneity as the explanation of sexuality? Comparative study shows that ancient asexual taxa are associated with both biotically and abiotically homogeneous environments.

Jan Toman,Jaroslav Flegr

doi:10.1002/ece3.3716

Abstract

Ecological theories of sexual reproduction assume that sexuality is advantageous in certain conditions, for example, in biotically or abiotically more heterogeneous environments. Such theories thus could be tested by comparative studies. However, the published results of these studies are rather unconvincing. Here, we present the results of a new comparative study based exclusively on the ancient asexual clades. The association with biotically or abiotically homogeneous environments in these asexual clades was compared with the same association in their sister, or closely related, sexual clades. Using the conservative definition of ancient asexuals (i.e., age >1 million years), we found eight pairs of taxa of sexual and asexual species, six differing in the heterogeneity of their inhabited environment on the basis of available data. The difference between the environmental type associated with the sexual and asexual species was then compared in an exact binomial test. The results showed that the majority of ancient asexual clades tend to be associated with biotically, abiotically, or both biotically and abiotically more homogeneous environments than their sexual controls. In the exploratory part of the study, we found that the ancient asexuals often have durable resting stages, enabling life in subjectively homogeneous environments, live in the absence of intense biotic interactions, and are very often sedentary, inhabiting benthos, and soil. The consequences of these findings for the ecological theories of sexual reproduction are discussed.

Highlights

Paradox of sexual reproductionThe term “sexual” may be assigned to a broad array of processes
After the identification of the AA groups and their sexual controls, we focused on the comparison of the character of their environments
Reviewing relevant literary resources, including several recent studies, we concluded that at least eight of the putative AA groups do fulfil our strict criteria of ancient asexuality: bdelloid rotifers (Bdelloidea), darwinulid ostracods (Darwinulidae), some mite lineages of the Oribatidae, Endeostigmata, and Trombidiformes, shoestring fern Vittaria appalachiana, some lineages of stick insects from the genus Timema, and some lineages of the bivalve genus Lasaea; see Supplemental table S1

Summary

Introduction

Paradox of sexual reproductionThe term “sexual” may be assigned to a broad array of processes (see e.g. Redfield, 2001; Birky, 2009; Gorelick & Carpinone, 2009; Schön et al, 2009a). Sexual reproduction (sensu amphimixis) is one of the most enigmatic phenomena in evolutionary biology, especially if its overwhelming predominance in eukaryotes is taken into account The reason is that it brings many obvious disadvantages in comparison to asexual reproduction—. An asexual lineage invading the sexual population would be expected to quickly drive its sexual conspecifics extinct (Maynard Smith, 1978). None of these disadvantages apply to all sexual species because of the highly variable nature of their reproduction. Under many circumstances, the disadvantages apply profoundly (Lehtonen et al, 2012). Sexual reproduction remains an enigma that calls for explanation

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