Transitions in sex determination and sex chromosomes across vertebrate species

Abstract

Despite the prevalence of sexual reproduction across eukaryotes, there is a remarkable diversity of sex-determination mechanisms. The underlying causes of this diversity remain unclear, and it is unknown whether there are convergent trends in the directionality of turnover in sex-determination mechanisms. We used the recently assembled Tree of Sex database to assess patterns in the evolution of sex-determination systems in the remarkably diverse vertebrate clades of teleost fish, squamate reptiles and amphibians. Contrary to theoretical predictions, we find no evidence that the evolution of separate sexes is irreversible, as transitions from separate sexes to hermaphroditism occur at higher rates than the reverse in fish. We also find that transitions from environmental sex determination to genetic sex determination occur at higher rates than the reverse in both squamates and fish, suggesting that genetic sex determination is more stable. However, our data are not consistent with the hypothesis that heteromorphic sex chromosomes are an "evolutionary trap." Rather, we find similar transition rates between homomorphic and heteromorphic sex chromosomes in both fish and amphibians, and to environmental sex determination from heteromorphic vs. homomorphic sex chromosome systems in fish. Finally, we find that transitions between male and female heterogamety occur at similar rates in amphibians and squamates, while transitions to male heterogamety occur at higher rates in fish. Together, these results provide the most comprehensive view to date of the evolution of vertebrate sex determination in a phylogenetic context, providing new insight into long-standing questions about the evolution of sexual reproduction.

Keywords: amphibians; fish; phylogenetic comparative methods; sex chromosome; sex determination; squamate reptiles.

Figure 1. The distribution of sex determination across three vertebrate clades

Species are coded as being either XY heteromorphic (dark blue), XY homomorphic (light blue), ZW heteromorphic (dark red), ZW homomorphic (light red), unknown homomorphic (?, gray), having environmental sex determination (ESD, green), or being hermaphrodites (yellow). Species that had some degree of ESD were classified as such, regardless of their chromosomes. Note that in the actual analyses we estimated parameters across 10 different datasets, with slightly different taxonomic coverage; for the purposes of this figure, we selected one of these at random.

Figure 2. Transitions from gonochorism to hermaphroditism occur at a higher rate than the reverse in fish

Posterior distribution of the difference in transition rates between gonochorism and hermaphroditism in fish. Across the 10 datasets, 94.9% of the posterior distribution supports the conclusion that transitions from gonochorism to hermaphroditism occur at a higher rate than the reverse.

Figure 3. Transitions from environmental sex determination to genetic sex determination occur at a higher rate than the reverse in fish and squamates

Posterior distribution of the difference in transition rates between genetic sex determination (GSD) and environmental sex determination (ESD) for fish (left panel) and squamates (right panel). Across the 10 datasets, 98.4% of the posterior distribution in fish and 100% of the posterior distribution in squamates supports the conclusion that transitions from ESD to GSD occur at a higher rate than the reverse. Indeed, across the posterior distribution, the rate of transition from ESD to GSD is, on average, around 6 (fish) and 17.3 (squamates) times higher than the reverse.

Figure 4. No differences in transition rates between homomorphic and heteromorphic sex chromosomes in either fish or amphibians

Posterior distribution of the difference in transition rates between homomorphic and heteromorphic sex chromosomes in fish (left panel) and amphibians (right panel). Across the 10 datasets, 69.9% of the posterior distribution in fish and 69.7% of the posterior distribution in amphibians support a higher rate of transitions from heteromorphic to homomorphic sex chromosomes than the reverse, but these results are not significant.

Figure 5. No difference in transition rate from homomorphic sex chromosomes to ESD versus heteromorphic sex chromosomes to ESD in fish

Posterior distribution of the difference in transition rates between homomorphic sex chromosomes and ESD, and heteromorphic sex chromosomes and ESD. Across the 10 datasets and the entire analyses, 43.7% of the posterior distribution supports a higher rate of transitions from heteromorphic sex chromosomes to ESD, but this is not significant. The posterior distributions of the transition rates between heteromorphic sex chromosomes and ESD and between homomorphic sex chromosomes and ESD are significantly greater than zero (Supplemental Figures 2 and 3).

Figure 6. Transitions from ZW to XY sex determination systems occur at a higher rate than the reverse in fish, but not in squamates or amphibians

Posterior distribution of the difference in transition rates between XY and ZW systems for fish (left panel), squamates (middle panel), and amphibians (right panel). Across the 10 datasets, 99.9% of the posterior distribution supports the conclusion that there is a higher rate of transitions from ZW to XY sex determination systems in fish. However, there is not significant support for this conclusion in other clades: only 77.9% of the posterior distribution in squamates and 56.0% of the posterior distribution in amphibians suggest a higher rate of transitions from ZW to XY sex determination systems than the reverse.