Department of Biological Sciences, Western Michigan University, 1903 W Michigan Ave., Kalamazoo, MI 49008, USA.
Bell Museum of Natural History, University of Minnesota, 100 Ecology, 1987 Upper Buford Circle, Saint Paul, MN 55108, USA.
Syst Biol. 2024 Oct 25;73(4):683-703. doi: 10.1093/sysbio/syae022.
Migration independently evolved numerous times in animals, with a myriad of ecological and evolutionary implications. In fishes, perhaps the most extreme form of migration is diadromy, the migration between marine and freshwater environments. Key and long-standing questions are: how many times has diadromy evolved in fishes, how frequently do diadromous clades give rise to non-diadromous species, and does diadromy influence lineage diversification rates? Many diadromous fishes have large geographic ranges with constituent populations that use isolated freshwater habitats. This may limit gene flow between some populations, increasing the likelihood of speciation in diadromous lineages relative to nondiadromous lineages. Alternatively, diadromy may reduce lineage diversification rates if migration is associated with enhanced dispersal capacity that facilitates gene flow within and between populations. Clupeiformes (herrings, sardines, shads, and anchovies) is a model clade for testing hypotheses about the evolution of diadromy because it includes an exceptionally high proportion of diadromous species and several independent evolutionary origins of diadromy. However, relationships among major clupeiform lineages remain unresolved, and existing phylogenies sparsely sampled diadromous species, limiting the resolution of phylogenetically informed statistical analyses. We assembled a phylogenomic dataset and used multi-species coalescent and concatenation-based approaches to generate the most comprehensive, highly resolved clupeiform phylogeny to date, clarifying associations among several major clades and identifying recalcitrant relationships needing further examination. We determined that variation in rates of sequence evolution (heterotachy) and base-composition (nonstationarity) had little impact on our results. Using this phylogeny, we characterized evolutionary patterns of diadromy and tested for differences in lineage diversification rates between diadromous, marine, and freshwater lineages. We identified 13 transitions to diadromy, all during the Cenozoic Era (10 origins of anadromy, 2 origins of catadromy, and 1 origin of amphidromy), and 7 losses of diadromy. Two diadromous lineages rapidly generated nondiadromous species, demonstrating that diadromy is not an evolutionary dead end. We discovered considerably faster transition rates out of diadromy than to diadromy. The largest lineage diversification rate increase in Clupeiformes was associated with a transition to diadromy, but we uncovered little statistical support for categorically faster lineage diversification rates in diadromous versus nondiadromous fishes. We propose that diadromy may increase the potential for accelerated lineage diversification, particularly in species that migrate long distances. However, this potential may only be realized in certain biogeographic contexts, such as when diadromy allows access to ecosystems in which there is limited competition from incumbent species.
动物中的迁徙现象独立进化了多次，这对生态和进化具有深远的影响。在鱼类中，也许最极端的迁徙形式是洄游，即海洋和淡水环境之间的迁徙。关键且长期存在的问题是：洄游在鱼类中进化了多少次，洄游类群产生非洄游物种的频率是多少，以及洄游是否会影响谱系多样化率？许多洄游鱼类的地理分布范围很广，组成种群的鱼类利用孤立的淡水栖息地。这可能会限制一些种群之间的基因流动，从而增加洄游谱系相对于非洄游谱系发生物种形成的可能性。或者，如果迁徙与增强的扩散能力相关，从而促进种群内部和种群之间的基因流动，那么迁徙可能会降低谱系多样化率。鲱形目（鲱鱼、沙丁鱼、鲱鱼和凤尾鱼）是检验有关洄游进化假说的模型类群，因为它包括极高比例的洄游物种和几次独立的洄游起源。然而，主要鲱形目谱系之间的关系仍未解决，并且现有的系统发育树对洄游物种的采样稀疏，限制了基于系统发育的统计分析的分辨率。我们组装了一个基因组数据集，并使用多物种聚合并联方法生成了迄今为止最全面、分辨率最高的鲱形目系统发育，阐明了几个主要类群之间的关联，并确定了需要进一步研究的顽固关系。我们确定，序列进化（异速进化）和碱基组成（非平稳性）的速率变化对我们的结果几乎没有影响。使用该系统发育树，我们描述了洄游的进化模式，并测试了洄游、海洋和淡水谱系之间谱系多样化率的差异。我们确定了 13 次向洄游的转变，全部发生在新生代（10 次溯河洄游起源，2 次降海洄游起源和 1 次两栖洄游起源），7 次失去洄游。两个洄游谱系迅速产生了非洄游物种，表明洄游并不是进化的死胡同。我们发现离开洄游的转变速度比进入洄游的转变速度快得多。鲱形目中最大的谱系多样化率增加与向洄游的转变有关，但我们几乎没有发现统计学证据表明，与非洄游鱼类相比，洄游鱼类的谱系多样化率更快。我们提出，洄游可能会增加谱系加速多样化的潜力，尤其是在那些长距离迁徙的物种中。然而，这种潜力可能仅在某些生物地理背景下实现，例如当洄游允许进入竞争程度有限的生态系统时。
