Correlates of substitution rate variation in a robust Procellariiform seabird phylogeny

Molecular substitution rates vary among branches and can lead to inaccurate reconstructions of evolutionary relationships and obscure the true phylogeny of affected clades. Body mass is often assumed to have a major influence on substitution rate, though other factors such as population size, life history traits, and flight demands are also thought to have an influence. Birds of the order Procellariiformes—which encompasses petrels, storm-petrels and albatrosses—show a striking 900-fold difference in body mass between the smallest and largest members, divergent life history traits, and substantial heterogeneity in mitochondrial substitution rates. Here, we used genome-scale nuclear DNA sequence data from 4365 ultraconserved element loci (UCEs) in 51 procellariiform species to examine whether phylogenetic reconstruction using genome-wide datasets is robust to the presence of rate heterogeneity, and to identify predictors of substitution rate variation. Our results provide a backbone phylogeny for procellariiform seabirds and resolves several controversies about the evolutionary history of the order, demonstrating that albatrosses are basal, storm-petrels are paraphyletic and diving petrels nestled within the Procellariidae. We find evidence of rate variation; however, all phylogenetic analyses using both concatenation and multispecies coalescent approaches recovered the same branching topology, including analyses implementing different clock models, and analyses of the most and least clock-like loci. Overall, we find that rate heterogeneity is little impacted by body mass and age at first breeding, but moderately impacted by longevity and hand-wing index, a proxy for wing shape and flight efficiency. Our results indicate that substitution rate may be the product of interactions among many, potentially taxon-specific, variables.

不同演化分支的分子替换速率存在差异，这可能导致演化关系重建结果失真，并模糊受影响类群的真实系统发育关系。尽管种群大小、生活史特征以及飞行需求等其他因素也被认为会对替换速率产生影响，但体重通常被视作影响替换速率的主要因素。鹱形目（Procellariiformes）鸟类涵盖海燕、暴风海燕与信天翁类群，其现存类群的体重差异可达900倍，生活史特征分化显著，且线粒体替换速率存在显著异质性。本研究采集了51种鹱形目鸟类的基因组规模核DNA序列数据，涉及4365个超保守元件位点（ultraconserved element loci，简称UCEs），以此探究基于全基因组数据集的系统发育重建是否可耐受替换速率异质性的影响，并筛选替换速率变异的预测因子。本研究结果为鹱形目海鸟构建了系统发育主干框架，解决了该类群演化历史中的若干争议：信天翁为基部类群，暴风海燕属于并系群，而潜水海燕则嵌套于鹱科（Procellariidae）之中。本研究检测到了替换速率变异的信号；不过，无论是采用串联拼接分析法还是多物种溯祖法，所有系统发育分析均得到了一致的分支拓扑结构，包括使用不同分子钟模型的分析，以及针对最符合和最不符合分子钟的位点开展的分析。总体而言，替换速率异质性几乎不受体重和首次繁殖年龄的影响，但受寿命和翼手指数的影响中等——翼手指数可作为翼形与飞行效率的替代指标。本研究结果表明，替换速率可能是多个（甚至可能是类群特异性的）变量相互作用的产物。