Comparative population genomics of cryptic speciation and adaptive divergence in Bicknell's and Gray-cheeked Thrushes (Aves: Catharus bicknelli and C. minimus) Journal: Genome Biology and Evolution. Catharus

Cryptic speciation may occur when reproductive isolation is recent or the accumulation of morphological differences between sister lineages is slowed by stabilizing selection preventing phenotypic differentiation. In North America, Bicknell's Thrush (Catharus bicknelli) and its sister species, the Gray-cheeked Thrush (Catharus minimus), are parapatrically breeding migratory songbirds, distinguishable in nature only by subtle differences in song and coloration, and were recognized as distinct species only inthe 1990s. Previous molecular studies have estimated that the species diverged ~120 - 420 thousand YBP and found very low levels of introgression despite their similarity and sympatry in the spring (prebreeding) migration. To further clarify the history, genetic divergence, genomic structure and adaptive processes in C. bicknelli and C. minimus, we sequenced and assembled high-coverage reference genomes of both species and re-sequenced genomes from population samples of C. bicknelli, C. minimus, and two individuals of the Swainson's Thrush (C. ustulatus). The genome of C. bicknelli exhibits markedly higher abundances of transposable elements compared to other Catharus and chicken. Demographic and admixture analyses confirm moderate genome-wide differentiation (F st = 0.10) and limited gene flow between C. bicknelli and C. minimus, but suggest a more recent divergence than estimates based on mtDNA. We find evidence of rapid evolution of the Z-chromosome and elevated divergence consistent with natural selection on genomic regions near genes involved with neuronal processes in C. bicknelli. These genomes are a useful resource for future investigations of speciation, migration, and adaptation in Catharus thrushes.

隐蔽物种形成（cryptic speciation）可发生于两类情形：一是生殖隔离新近形成，二是稳定选择（stabilizing selection）抑制了表型分化（phenotypic differentiation），进而减缓姊妹支系间形态差异的累积。在北美地区，比氏鸫（Bicknell's Thrush，*Catharus bicknelli*）与其姊妹物种灰颊鸫（Gray-cheeked Thrush，*Catharus minimus*）为邻域繁殖的迁徙鸣禽，仅能通过鸣唱与羽色的细微差异在野外区分，二者直至20世纪90年代才被认定为独立物种。既往分子生物学研究估算，这两个物种的分化时间距今约12万至42万年（YBP，years before present），尽管它们在春季繁殖前迁徙阶段会出现同域分布且形态相似，但仅检测到极低水平的基因渐渗（introgression）。为进一步阐明比氏鸫与灰颊鸫的演化历史、遗传分化、基因组结构与适应性进程，本研究对两个物种的高覆盖度参考基因组进行了测序与组装，并对种群样本中的比氏鸫、灰颊鸫，以及2只斯温氏鸫（Swainson's Thrush，*Catharus ustulatus*）的基因组进行了重测序。相较于其他鸫属鸟类与鸡的基因组，比氏鸫的基因组中转座元件（transposable element）的丰度显著更高。种群历史与基因交流分析证实，比氏鸫与灰颊鸫之间存在中等程度的全基因组分化（Fst = 0.10）与有限的基因流，但提示二者的分化时间比基于线粒体DNA（mtDNA，mitochondrial DNA）的估算结果更近。本研究发现比氏鸫的Z染色体存在快速演化的证据，且其基因组中与神经过程相关基因邻近的区域呈现升高的分化水平，这与自然选择作用于这些区域的结论相符。上述基因组资源将为日后针对鸫属鸣禽的物种形成、迁徙演化与适应性进化的相关研究提供重要支撑。