ZW, XY, and yet ZW: Sex chromosome evolution in snakes even more complicated

Abstract

Snakes are historically important in the formulation of several central concepts on the evolution of sex chromosomes. For over 50 years, it was believed that all snakes shared the same ZZ/ZW sex chromosomes, which are homomorphic and poorly differentiated in "basal" snakes such as pythons and boas, while heteromorphic and well differentiated in "advanced" (caenophidian) snakes. Recent molecular studies revealed that differentiated sex chromosomes are indeed shared among all families of caenophidian snakes, but that boas and pythons evolved likely independently male heterogamety (XX/XY sex chromosomes). The historical report of heteromorphic ZZ/ZW sex chromosomes in a boid snake was previously regarded as ambiguous. In the current study, we document heteromorphic ZZ/ZW sex chromosomes in a boid snake. A comparative approach suggests that these heteromorphic sex chromosomes evolved very recently and that they are poorly differentiated at the sequence level. Interestingly, two snake lineages with confirmed male heterogamety possess homomorphic sex chromosomes, but heteromorphic sex chromosomes are present in both snake lineages with female heterogamety. We point out that this phenomenon is more common across squamates. The presence of female heterogamety in non-caenophidian snakes indicates that the evolution of sex chromosomes in this lineage is much more complex than previously thought, making snakes an even better model system for the evolution of sex chromosomes.

Landscape of snake’ sex chromosomes evolution spanning 85 MYR reveals ancestry of sequences despite distinct evolutionary trajectories

“…A similar pattern was observed in the Sanziniidae family, a sister group to Boidae (Fig. 8 ) 32 , but the Z and W chromosomes of Acrantophis sp. cf.…”

“…Caenophidia is a monophyletic group that contains over 80% of all the extant species of snakes, commonly referred as “ Advanced Snakes ”) 30 , 31 , 39 , 41 . On the other hand, well-differentiated sex chromosomes are more common in the more recently diversified groups of snakes, the advanced lineages 25 , but also present in the former groups of snakes as Typhlopoidea and Booidea 32 , 42 . The molecular and cytogenetic mechanisms of evolution of homomorphic sex chromosomes in snakes have not been the subject of rigorous studies compared to well-differentiated ones.…”

Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation

“…The traditional predictions are also not supported by the empirical data in other squamate lineages. A higher degree of differentiation in lineages with female heterogamety in comparison to male heterogamety was observed within snakes [82], chameleons [36,37], and between closely related teiid and lacertid lizards (20,83). On the other hand, XX/XY sex chromosomes are highly differentiated in viviparous mammals and iguanas [with the exception of basilisks 76,84]; however, sex chromosomes in these two groups are among the oldest sex chromosomes uncovered to date in amniotes and have thus potentially had a longer time to differentiate [85,86].…”

ZZ/ZW Sex Determination with Multiple Neo-Sex Chromosomes is Common in Madagascan Chameleons of the Genus Furcifer (Reptilia: Chamaeleonidae)

“…In any case, it seems that highly differentiated sex chromosomes tend to be evolutionary stable and recent molecular evidence disputed earlier reported transitions from GSD with highly differentiated sex chromosomes to ESD [15,16]. On the other hand, poorly differentiated sex chromosomes in reptiles, e.g., in boas and pythons [17,18], tend to be prone to sex chromosome turnovers, but it is not yet clear whether they can be replaced only with other GSD systems or with ESD as well. More accurate testing of these scenarios is currently prevented by the lack of primary data on sex determination in most reptilian lineages.…”