Disentangling the contemporary and historical effects of landscape on population genomic variation of two bird species restricted to the highland forest enclaves of northeastern Brazil

Investigating the impact of landscape features on patterns of genetic
variation is crucial to understand spatially dependent evolutionary
processes. Here, we assess the population genomic variation of two bird
species (Conopophaga cearae and Sclerurus cearensis) through the Caatinga
moist forest enclaves in northeastern Brazil. To infer the evolutionary
dynamics of bird populations through the Late Quaternary, we used
genome-wide polymorphism data obtained from double-digestion
restriction-site-associated DNA sequencing (ddRADseq), and integrated
population structure analyses, historical demography models,
paleodistribution modeling, and landscape genetics analyses. We found the
population differentiation among enclaves to be significantly related to
the geographic distance and historical resistance across the rugged
landscape. The climate changes at the end of the Pleistocene to the
Holocene likely triggered synchronic population decline in all enclaves
for both species. Our findings revealed that both geographic distance and
historical connectivity through highlands are important factors that can
explain the current patterns of genetic variation. Our results further
suggest that levels of population differentiation and connectivity cannot
be explained purely on the basis of contemporary environmental conditions.
By combining historical demographic analyses and niche modeling
predictions in a historical framework, we provide strong evidence that
climate fluctuations of the Quaternary promoted population differentiation
and a high degree of temporal synchrony among population size changes in
both species.

探究景观特征对遗传变异模式的影响，对于理解空间依赖性进化过程至关重要。本研究针对巴西东北部卡廷加（Caatinga）湿润森林飞地中的两种鸟类（Conopophaga cearae与Sclerurus cearensis）的种群基因组变异展开评估。为推演晚第四纪以来鸟类种群的进化动态，本研究采用双酶切限制性位点相关DNA测序（double-digestion restriction-site-associated DNA sequencing, ddRADseq）获取的全基因组多态性数据，并整合了种群结构分析、历史种群动力学模型、古分布区建模以及景观遗传学分析手段。研究发现，各飞地间的种群分化与地理距离及崎岖景观中的历史抗性呈显著相关。更新世末期至全新世的气候波动，或引发了两个物种种群在所有飞地中同步的种群衰退。本研究结果表明，地理距离与通过高地实现的历史连通性均为解释当前遗传变异模式的关键因素。研究结果进一步显示，种群分化与连通性水平无法仅通过当代环境条件得到合理解释。通过在历史框架下整合历史种群动力学分析与生态位建模预测，本研究为第四纪气候波动推动两个物种种群分化，以及种群数量变化呈现高度时间同步性提供了有力证据。