Richmond Jonathan Q, Gottscho Andrew D, Jockusch Elizabeth L, Leaché Adam D, Fisher Robert N, Reeder Tod W
U.S. Geological Survey, San Diego, CA, United States.
Department of Biology, San Diego State University, San Diego, CA, United States.
Evolution. 2025 Jul 18;79(7):1386-1399. doi: 10.1093/evolut/qpaf059.
Parallel evolution of the same reproductive isolation barrier within a taxon is an indicator of ecology's role in speciation (i.e., parallel speciation), yet spatiotemporal variability in the efficacy of the barrier can present challenges to retracing how it evolved. Here, we revisit the evidence for a candidate example of parallel speciation in a clade of scincid lizards (the Plestiodon skiltonianus complex) using genomic data, with emphasis on determining whether hybridization may have confounded the phylogenetic signals of parallelism for this group. Our results show a striking case of genealogical discordance, in which mitochondrial loci support multiple origins of a derived large-bodied morphotype (Plestiodon gilberti) within a small-bodied ancestor (Plestiodon skiltonianus), whereas nuclear loci indicate a single origin. We attribute the discordance to separate, temporally-spaced hybridization events that led to asymmetric capture of P. skiltonianus mitochondria in different regional lineages of P. gilberti. Nuclear introgression showed a similar directional bias but was less pervasive. We demonstrate how a mechanical reproductive barrier previously identified for this group explains the asymmetry of mitochondrial introgression, given that hybrid matings are most likely when the male is P. gilberti and the female is P. skiltonianus. We then use permutation tests of morphological data to provide evidence that the mechanical barrier is less stringent in areas where hybridization is inferred to have occurred. Our results demonstrate how biased hybridization can dictate which genetic variants are transmitted between species and emphasize the importance of accounting for introgression and deep coalescence in identifying phyletic signatures of parallel speciation.
一个分类单元内相同生殖隔离屏障的平行进化是生态在物种形成中所起作用的一个指标（即平行物种形成），然而该屏障功效的时空变异性可能给追溯其进化过程带来挑战。在这里，我们利用基因组数据重新审视了石龙子蜥蜴一个分支（斯氏石龙子复合体）中平行物种形成候选例子的证据，重点是确定杂交是否可能混淆了该类群平行性的系统发育信号。我们的结果显示了一个显著的谱系不一致案例，其中线粒体基因座支持在一个小型祖先（斯氏石龙子）内一个衍生的大体型形态（吉尔伯特石龙子）有多个起源，而核基因座表明只有一个起源。我们将这种不一致归因于不同时间间隔的单独杂交事件，这些事件导致在吉尔伯特石龙子的不同区域谱系中不对称地捕获了斯氏石龙子的线粒体。核基因渐渗显示出类似的方向偏差，但分布范围较小。鉴于当雄性为吉尔伯特石龙子而雌性为斯氏石龙子时杂交交配最有可能发生，我们证明了先前为该类群确定的一个机械生殖屏障如何解释线粒体渐渗的不对称性。然后我们使用形态学数据的置换检验来提供证据，表明在推断发生杂交的区域，机械屏障不那么严格。我们的结果证明了有偏差的杂交如何决定哪些遗传变异在物种间传递，并强调了在识别平行物种形成的系统发育特征时考虑基因渐渗和深度聚合的重要性。
