Phylogeography, more than elevation, accounts for sex-chromosome differentiation in Swiss populations of the common frog (Rana temporaria)

Sex chromosomes in vertebrates range from highly heteromorphic (as in most birds and mammals) to strictly homomorphic (as in many fishes, amphibians, and non-avian reptiles). Reasons for these contrasted evolutionary trajectories remain unclear, but species such as common frogs with polymorphism in the extent of sex-chromosome differentiation may potentially deliver important clues. By investigating 92 common-frog populations from a wide range of elevations throughout Switzerland, we show that sex-chromosome differentiation strongly correlates with alleles at the candidate sex-determining gene Dmrt1. Y-specific Dmrt1 haplotypes cluster into two main haplogroups, YA and YB, with a phylogeographic signal that parallels mtDNA haplotypes: YA populations, with mostly well-differentiated sex chromosomes, occur primarily south of the main alpine ridge that bisects Switzerland, while YB populations, with mostly undifferentiated (proto-)sex chromosomes, occur north of this ridge. Elevation has only a marginal effect, opposing previous suggestions of a major role for climate on sex-chromosome differentiation. The Y-haplotype effect might result from differences in the penetrance of alleles at the sex-determining locus (such that sex reversal and ensuing X-Y recombination are more frequent in YB populations), and/or fixation of an inversion on YA (as supported by the empirical observation that YA haplotypes might not recombine in XYA females).

脊椎动物的性染色体变异范围极广，从高度异形（如多数鸟类和哺乳类）到严格同形（如多数鱼类、两栖类及非鸟类爬行类）。这类截然不同的演化路径的成因至今尚未明晰，但普通蛙这类在性染色体分化程度上存在多态性的物种，或可提供关键研究线索。本研究针对瑞士境内覆盖不同海拔梯度的92个普通蛙种群开展调查，结果显示性染色体分化程度与候选性别决定基因Dmrt1的等位基因存在显著相关性。Y染色体特异性Dmrt1单倍型可聚类为两个主要单倍群——YA与YB，二者的系统地理信号与线粒体DNA（mtDNA）单倍型高度契合：以高度分化性染色体为特征的YA种群，主要分布在横贯瑞士的阿尔卑斯主山脊以南；而以未分化（原始）性染色体为特征的YB种群，则分布于该山脊以北。海拔对性染色体分化的影响仅为边际效应，这与此前提出的“气候对性染色体分化起主要调控作用”的观点相悖。Y单倍型的效应可能源于两方面：一是性别决定位点等位基因的外显率差异（这使得YB种群中性逆转及随之发生的X-Y重组更为频繁）；二是YA单倍群上存在固定的染色体倒位，该假说得到了实证观测的支撑：XYA型雌性体内的YA单倍型可能无法发生重组。