Evolutionary transitions between mechanisms of sex determination in vertebrates

Abstract

Sex in many organisms is a dichotomous phenotype-individuals are either male or female. The molecular pathways underlying sex determination are governed by the genetic contribution of parents to the zygote, the environment in which the zygote develops or interaction of the two, depending on the species. Systems in which multiple interacting influences or a continuously varying influence (such as temperature) determines a dichotomous outcome have at least one threshold. We show that when sex is viewed as a threshold trait, evolution in that threshold can permit novel transitions between genotypic and temperature-dependent sex determination (TSD) and remarkably, between male (XX/XY) and female (ZZ/ZW) heterogamety. Transitions are possible without substantive genotypic innovation of novel sex-determining mutations or transpositions, so that the master sex gene and sex chromosome pair can be retained in ZW-XY transitions. We also show that evolution in the threshold can explain all observed patterns in vertebrate TSD, when coupled with evolution in embryonic survivorship limits.

Did sex chromosome turnover promote divergence of the major mammal groups?

“…There are phylogenies of closely related agamid lizards that reveal at least four flip‐flops through genetic sex determination (GSD) and temperature sex determination (TSD), generating novel sex chromosomes 27. Some reptile species have sex chromosome systems that can be overridden by temperature 28, 29; these dual systems are extremely labile, able to change rapidly to TSD systems and even between ZW and XY 30, 31. Similar GSD‐TSD transitions may be common in some fish and may also facilitate changes in sex determination 32, 33, 34.…”

Molecular basis and genetic improvement of economically important traits in aquaculture animals

“…In mammals, primary sex determination genes have been divided into 4 classes, in which class I comprises Y genes that have a male-specific effect required for spermatogenesis, class II are X genes that are expressed at a higher level in females than in males by virtue of the 2:1 ratio, class III are X genes that receive a parental imprint, and class IV are sex-specific regions of heterochromatin that exert effects on the epigenetic status of the rest of the genome [87]. Of course, sex determination mechanisms are also intricate in fishes, because fishes, like other aquatic animals of amphibians and reptiles, include male or female heterogametic genetic sex determination with or without strongly differentiated sex chromosomes [88,89]. A recent report indicates that sex-chromosome homomorphy in European tree frogs does not result from a recent turnover but is maintained over evolutionary timescales by occasional X-Y recombination, implicating that seemingly ever-young sex chromosomes may thus carry old-established sex-determining genes [90].…”

Dmrt1 induces the male pathway in a turtle with temperature-dependent sex determination

“…In particular, little is known about (1) which genetic components are responsible for triggering the differentiation of bipotential primordium into either a testis or ovary; and (2) how the physical signal of temperature is transduced into a biological signal. Phylogenetic analyses suggest frequent and repeated evolutionary transitions between TSD and genetic sex determination (GSD) in environmentally sensitive lineages, including reptiles (Quinn et al, 2011;Sarre et al, 2011). In many cases, both GSD and TSD simultaneously exist in the same species Radder et al, 2008;Yamamoto et al, 2014).…”