Reconstructing the History of Anole Sex Chromosomes

Gorman_Dominica_1965_Anolis_oculatus

George Gorman in Dominica

In the 1960s and 70’s evolutionary cytogenetics experienced a remarkable burst of interest and scholarship. Thanks largely to the efforts of George Gorman (at right) and others working at the Museum of Comparative Zoology, anoles played a central role in this research (some historical detail has previously been posted on AA). Among their findings was the occurrence of heteromorphic sex chromosomes, sex chromosomes that are visibly distinguishable from each other under a microscope, in several Anolis species but not others. Furthermore, Gorman and colleagues discovered that those Anolis species with heteromorphic sex chromosomes all had male heterogamety, with some having an XX/XY system while others had an XXXX/XXY system. Chromosomes from nearly 100 Anolis species were examined during this period and about 1/3 of those species had heteromorphic sex chromosomes. Interest in chromosome evolution waned in the 1980’s as DNA sequence data became increasing accessible, but there has been a recent resurgence thanks, in part, to sex chromosomes.

Sex chromosomes have received increased attention from evolutionary biologists because they seem to play a special role in adaption and speciation in addition to their involvement in sex determination.  Therefore understanding how sex chromosomes evolve can bear light on these core evolutionary processes. Among vertebrates the study of sex chromosomes has largely focused on a few lineages: mammals, birds, and snakes. Within each of these clades, species share conserved, ancestrally derived sex-determining loci and have little or no variation in their sex chromosome complements, the set of chromosomes that segregate with sex (male heterogamy – XY in mammals, or female heterogamy – ZW in birds and snakes). In contrast, teleost fishes, frogs and geckos have experienced repeated turnover in their sex determining loci, in other words a new sex determining locus has evolved in some species and replaced the ancestral one. These lineages also have a variety of sex chromosome complements. Like these taxa anoles exhibit a variety of sex chromosome complements (XY, XXY and homomorphic sex chromosomes) but it remained to be determined if the sex determining loci in anoles are conserved or have experienced turnover.

In a recent paper, in Evolution, Tony Gamble and colleagues (myself included) used the wealth of anole karyotype data and resources derived from the A. carolinensis genome to ask if the variation in sex chromosome complement reflects a history of sex chromosome stability or turnover. We showed that even though most Anolis species lack heteromorphic sex chromosomes, all species in the genus likely have sex chromosomes with male heterogamety. The X and Y in most species are simply not morphologically distinguishable. We also found that Anolis sex chromosomes are derived from a single ancestral pair of autosomes. We came to these conclusions combining multiple analyses and independent sources of data including phylogenetic comparative analyses, cytogenetics, and molecular genetics. As a bonus we generated a new molecular phylogeny to explore Anolis karyotype evolution. This new evolutionary tree included 216 species – the most Anolis species sampled in a molecular phylogeny to date. In a scenario that has played out often in the history of evolutionary biology (see Darwin and Wallace or Kimura and King & Jukes for prominent examples) another study, recently accepted to Evolution, used some of the same molecular genetic techniques (qPCR) to reach similar conclusions.

chromo_tree

Distribution of sex chromosome complements on a pruned phylogeny of anoles. Circles at tips represent sex chromosome complement: orange – XY, blue – XXY and green represents species with cytogenetically indistinguishable sex chromosomes. Cytogenetic analyses were performed on species with stars.

Anolis sex chromosomes, like the sex chromosomes of birds, mammals, and snakes, are derived from a single ancestral chromosome pair. Unlike these other clades, the sex chromosomes of anoles have not all degenerated to such a degree that they are heteromorphic. Anolis sex chromosomes can also provide a nice model to investigate Y chromosome degeneration (or lack thereof) in a large, species rich clade. Furthermore, it will be interesting to see if evolutionary processes influenced by heteromorphic sex chromosomes (such as Haldane’s Rule, and sex-specific adaptation) hold up equally as well in lineages with homomorphic sex chromosomes.

About Anthony Geneva

Postdoctoral Fellow at Harvard University. I use a variety of evolutionary genetic approaches to ask questions about gene flow, adaptation and speciation.

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