Ever-Young Sex Chromosomes in European Tree Frogs

Non-recombining sex chromosomes are expected to undergo evolutionary decay, ending up genetically degenerated, as has happened in birds and mammals. Why are then sex chromosomes so often homomorphic in cold-blooded vertebrates? One possible explanation is a high rate of turnover events, replacing master sex-determining genes by new ones on other chromosomes. An alternative is that X-Y similarity is maintained by occasional recombination events, occurring in sex-reversed XY females. Based on mitochondrial and nuclear gene sequences, we estimated the divergence times between European tree frogs (Hyla arborea, H. intermedia, and H. molleri) to the upper Miocene, about 5.4–7.1 million years ago. Sibship analyses of microsatellite polymorphisms revealed that all three species have the same pair of sex chromosomes, with complete absence of X-Y recombination in males. Despite this, sequences of sex-linked loci show no divergence between the X and Y chromosomes. In the phylogeny, the X and Y alleles cluster according to species, not in groups of gametologs. We conclude that sex-chromosome homomorphy in these tree frogs does not result from a recent turnover but is maintained over evolutionary timescales by occasional X-Y recombination. Seemingly young sex chromosomes may thus carry old-established sex-determining genes, a result at odds with the view that sex chromosomes necessarily decay until they are replaced. This raises intriguing perspectives regarding the evolutionary dynamics of sexually antagonistic genes and the mechanisms that control X-Y recombination.非重组性染色体预计将经历进化衰退，最终发生遗传退化，这一过程在鸟类和哺乳动物中已有实例。但为何冷血脊椎动物的性染色体往往保持同态形态？一种可能的解释是存在高频的性染色体更替事件：即通过其他染色体上的新基因取代原有主性别决定基因。另一种可能性则是，X-Y序列的相似性可通过偶尔发生在性反转XY雌性中的重组事件得以维持。基于线粒体与核基因序列，我们估算了欧洲雨蛙（Hyla arborea、H. intermedia与H. molleri）之间的分化时间，其分歧可追溯至中新世晚期，距今约540万至710万年。针对微卫星多态性的同胞关系分析显示，这三个物种拥有同一对性染色体，且雄性个体中完全不存在X-Y重组现象。尽管如此，性连锁位点的序列并未呈现X与Y染色体间的分化差异。在系统发育树中，X与Y等位基因按物种类群聚类，而非按配子同源基因分组。我们由此得出结论：这些雨蛙的性染色体同态并非源于近期的性染色体更替事件，而是在进化时间尺度上通过偶尔发生的X-Y重组得以维持。因此，看似年轻的性染色体或许携带着古老的性别决定基因，这一结果与"性染色体必然衰退直至被取代"的传统观点相悖。该发现为性拮抗基因的进化动力学以及调控X-Y重组的分子机制带来了极具启发性的研究视角。