Sperm‐dependent asexual species and their role in ecology and evolution

Abstract

Sexual reproduction is the primary mode of reproduction in eukaryotes, but some organisms have evolved deviations from classical sex and switched to asexuality. These asexual lineages have sometimes been viewed as evolutionary dead ends, but recent research has revealed their importance in many areas of general biology. Our review explores the understudied, yet important mechanisms by which sperm‐dependent asexuals that produce non‐recombined gametes but rely on their fertilization, can have a significant impact on the evolution of coexisting sexual species and ecosystems. These impacts are concentrated around three major fields. Firstly, sperm‐dependent asexuals can potentially impact the gene pool of coexisting sexual species by either restricting their population sizes or by providing bridges for interspecific gene flow whose type and consequences substantially differ from gene flow mechanisms expected under sexual reproduction. Secondly, they may impact on sexuals' diversification rates either directly, by serving as stepping‐stones in speciation, or indirectly, by promoting the formation of pre‐ and postzygotic reproduction barriers among nascent species. Thirdly, they can potentially impact on spatial distribution of species, via direct or indirect (apparent) types of competition and Allee effects. For each such mechanism, we provide empirical examples of how natural sperm‐dependent asexuals impact the evolution of their sexual counterparts. In particular, we highlight that these broad effects may last beyond the tenure of the individual asexual lineages causing them, which challenges the traditional perception that asexual lineages are short‐lived evolutionary dead ends and minor sideshows. Our review also proposes new research directions to incorporate the aforementioned impacts of sperm‐dependent asexuals. These research directions will ultimately enhance our understanding of the evolution of genomes and biological interactions in general.

Absence of female preference and the origin of a unisexual species, the Amazon molly (Poecilia formosa)

“…Clearly, in the case of the Amazon molly, some breakdown of isolation must have happened. We know this through the existence of Amazon mollies, but other such breakdowns may not leave behind such a large footprint (Janko et al, 2018(Janko et al, , 2023. Indeed, while reports of actual hybrids between mollies in nature are rare, there is mounting evidence for a bigger role of hybridization than previously assumed (Moran et al, 2021;Schwenk et al, 2008).…”

“…It should be noted that in species that are sperm dependent (all asexual hybrid fishes and amphibians), the ecology of their establishment and maintenance is particularly complicated to explain in an eco-evolutionary framework, given their need to coexist with (but not outcompete) their sexual sperm donors, among other effects (Cerepaka & Schlupp, 2023;Janko et al, 2023;Riesch et al, 2012).…”

“…Once established, asexual hybrids play important ecological roles, for example, via resource competition with coexisting sexual species, or even in speciation of sexual species (Janko et al, 2023;Vrijenhoek, 1994). Asexual Amazon mollies (P. formosa) show almost complete niche overlap with their sexual hosts, for example, when it comes to feeding Scharnweber, Plath, Winemiller, et al, 2011), or parasite load (Tobler & Schlupp, 2005).…”