Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum'

Abstract

We review knowledge about the roles of sex chromosomes in vertebrate hybridization and speciation, exploring a gradient of divergences with increasing reproductive isolation (speciation continuum). Under early divergence, well-differentiated sex chromosomes in meiotic hybrids may cause Haldane-effects and introgress less easily than autosomes. Undifferentiated sex chromosomes are more susceptible to introgression and form multiple (or new) sex chromosome systems with hardly predictable dominance hierarchies. Under increased divergence, most vertebrates reach complete intrinsic reproductive isolation. Slightly earlier, some hybrids (linked in ‘the extended speciation continuum') exhibit aberrant gametogenesis, leading towards female clonality. This facilitates the evolution of various allodiploid and allopolyploid clonal (‘asexual’) hybrid vertebrates, where ‘asexuality' might be a form of intrinsic reproductive isolation. A comprehensive list of ‘asexual' hybrid vertebrates shows that they all evolved from parents with divergences that were greater than at the intraspecific level (K2P-distances of greater than 5–22% based on mtDNA). These ‘asexual' taxa inherited genetic sex determination by mostly undifferentiated sex chromosomes. Among the few known sex-determining systems in hybrid ‘asexuals', female heterogamety (ZW) occurred about twice as often as male heterogamety (XY). We hypothesize that pre-/meiotic aberrations in all-female ZW-hybrids present Haldane-effects promoting their evolution. Understanding the preconditions to produce various clonal or meiotic allopolyploids appears crucial for insights into the evolution of sex, ‘asexuality' and polyploidy. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

Lizards as Model Organisms of Sex Chromosome Evolution: What We Really Know from a Systematic Distribution of Available Data?

“…It thus appears clear that, while recent studies and different methodological approaches greatly improved our knowledge on sex chromosome systems in lizards, a good portion of their systematic distribution remains unexplored. Multiple times, the amount and diversity of available data has been indicated as the main limiting factor in our knowledge of sex chromosome systems [ 153 , 154 , 155 ], and future analyses focused on completely unstudied and highly undersampled lizard families would help to greatly improve our understanding of mechanisms of sex chromosome evolution in vertebrates.…”

Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

“…Hybrids of parental species with higher divergence may exhibit sex-specific distortions of gametogenesis typified by potential male sterility and frequently female clonality, often closely linked to polyploidization [67][68][69]. Most of these hemiclonal, clonal and meroclonal (Glossary in [64]) vertebrates of hybrid-origin evolved in parental GSD lineages with undifferentiated sex chromosomes under male (XY) or-probably more frequently-female heterogamety (ZW) [64]. The emergence of a new sex-determining system might be linked to allopolyploidization [64,70] (case 21 in figure 2).…”

“…Most of these hemiclonal, clonal and meroclonal (Glossary in [64]) vertebrates of hybrid-origin evolved in parental GSD lineages with undifferentiated sex chromosomes under male (XY) or-probably more frequently-female heterogamety (ZW) [64]. The emergence of a new sex-determining system might be linked to allopolyploidization [64,70] (case 21 in figure 2). Improving our understanding of the genomic preconditions that facilitate the generation of such hybrid clonal or allopolyploid vertebrates appears crucial for insights into the evolution of vertebrate sex, hybrid-origin gametogenetic aberrations, polyploidy and speciation.…”

“…It is thus well established that differentiated sex chromosomes contribute significantly to speciation and affect hybridization and introgression [61][62][63]. However, these effects remain largely unexplored in systems with poorly differentiated sex chromosomes [64]. Haldane's effects may lead to less introgression of loci linked to well-differentiated sex chromosomes across hybrid zones in comparison to autosomes.…”

Preface

“…-Co-option of the same linkage groups into sex chromosomes [15,16]; -Is differentiation of sex chromosomes a unidirectional pathway? [17,18]; -Consequences of differentiated sex chromosomes [19]; -Differences in differentiation of sex chromosomes under male versus female heterogamety [20,21]; -Evolution of sex chromosomes under hybridization and polyploidy [23][24].…”