Why Do Hybrids Turn Down Sex?

Abstract

Asexual reproduction is ancestral in prokaryotes; the switch to sexuality in eukaryotes is one of the major transitions in the history of life. The study of the maintenance of sex in eukaryotes has raised considerable interest for decades and is still one of evolutionary biology's most prominent question. The observation that many asexual species are of hybrid origin have led some to propose that asexuality in hybrids results from sexual processes being disturbed because of incompatibilities between the two parental species' genomes. This proximate theory appears difficult in real life, as it requires fundamental reproductive traits to be profoundly altered without collapsing individuals' fertility. Repeated failures to produce asexual Amazon Molly in the lab through crossing experiments show that we are still in need of an evolutionary explanation. Here, we present a mathematical model and propose an adaptive route for the evolution of asexuality from previously sexual hybrids. Under smaller reproductive alterations, we show that asexuality can evolve to rescue hybrids' reproduction. Importantly, we highlight that when incompatibilities only affect the fusion of sperm and egg's genomes, unreduced meiosis and paternal genome elimination can evolve separately, greatly facilitating the overall evolutionary route.

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

“…This was suggested by Alberici da as an early stage of the evolution of the Amazon molly and subsequently modeled by Fyon et al (2023). This pathway, however, is not compatible with genomic data showing a single hybrid origin of the Amazon molly (Warren et al, 2018).…”

“…In general, the resulting asexual modes of reproduction are genetically totally (parthenogenesis and gynogenesis) or partially (hybridogenesis) clonal, involve unreduced eggs, and sometimes require sperm to trigger embryogenesis (Avise, 2008;Suomalainen et al, 1987). The evolutionary pathway to emergence of these asexual species is still highly debated: though it is often thought that asexuality appears readily as a direct and immediate result of hybridization (Schlupp, 2005), it has been proposed that asexuality can evolve from sexual hybrids through multiple small and incremental evolutionary steps (Fyon et al, 2023).…”

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

“…Rutilus rutilus × Abramis bramma (Slyn'ko, 2000). Fyon et al (2023) suggested that the establishment of a spermdependent parthenogen may be more complex and numerous fundamental traits may evolve gradually. For instance, while the ability to produce unreduced gametes may emerge "instantaneously" as a result of hampered crosstalk between diverged parental genomes (Marta et al, 2023), others, like the ability to reject sperm's genome after fertilization, may evolve subsequently.…”

“…Because of their atypical meiosis and non‐Mendelian propagation of genomes, obligate asexuals serve as excellent models for understanding fundamental questions in evolution, ecology, and cell biology (e.g., Bengtsson, 2009; Brockhurst et al, 2014; Dalziel et al, 2020; Laskowski et al, 2019; Lively & Morran, 2014; Meirmans, 2009; Van Valen, 1973). Although seemingly rare compared to sexuals, they evolved independently in different taxonomic groups of metazoans (Fyon et al, 2023), suggesting this trait has high relevance for evolution and represents a fascinating challenge to what we understand as “typical” reproductive mode and sex.…”