Long-term climatic stability drives accumulation and maintenance of divergent lineages in a temperate biodiversity hotspot

Anthropogenic climate change is forecast to drive regional climate disruption and instability across the globe. These impacts are likely to be exacerbated within biodiversity hotspots, both due to the greater potential for species loss but also to the possibility that endemic lineages might not have experienced significant climatic variation in the past, limiting their evolutionary potential to respond to rapid climate change. We assessed the role of climatic stability on the accumulation and persistence of lineages in an obligate freshwater fish group endemic to the southwest Western Australia (SWWA) biodiversity hotspot. Using 19,426 genomic (ddRAD-seq) markers and species distribution modelling, we explored the phylogeographic history of western (Nannoperca vittata) and little (Nannoperca pygmaea) pygmy perches, assessing population divergence and phylogenetic relationships, delimiting species and estimating changes in species distributions from the Pliocene to 2100. We identified two deep phylogroups comprising three divergent clusters, which showed no historical connectivity since the Pliocene. We conservatively suggest these represent three isolated species with additional intraspecific structure within one widespread species. All lineages showed long-term patterns of isolation and persistence owing to climatic stability but with significant range contractions likely under future climate change. Our results highlighted the role of climatic stability in allowing the persistence of isolated lineages in the SWWA. This biodiversity hotspot is under compounding threat from ongoing climate change and habitat modification, which may further threaten previously undetected cryptic diversity across the region.

人为气候变化预计将在全球范围内引发区域性气候紊乱与不稳定。此类影响在生物多样性热点（biodiversity hotspot）区域可能进一步加剧：一方面源于该区域物种丧失的风险更高，另一方面则是由于特有演化支系在过往或许未曾经历显著的气候波动，进而限制了其应对快速气候变化的演化潜力。我们针对澳大利亚西南部（southwest Western Australia, SWWA）生物多样性热点区域特有的专性淡水鱼类类群，评估了气候稳定性对演化支系积累与存续的调控作用。本研究依托19426个基因组（ddRAD-seq）标记与物种分布模型，探究了西部侏儒鲈（*Nannoperca vittata*）与矮身侏儒鲈（*Nannoperca pygmaea*）的系统地理历史，分析了种群分化与系统发育关系，完成了物种界定，并估算了从上新世（Pliocene）至2100年的物种分布变化。研究识别出两个深源系统支群，包含三个分化显著的聚类类群，二者自上新世以来便未发生过历史基因交流。我们保守推断，这些类群代表三个孤立物种，其中一个广布物种内部还存在额外的种内结构。所有支系均表现出因气候稳定而形成的长期隔离与存续模式，但在未来气候变化情景下，其分布范围很可能出现显著收缩。本研究结果凸显了气候稳定性在澳大利亚西南部生物多样性热点区域维持孤立演化支系存续中的关键作用。该生物多样性热点区域正面临气候变化与栖息地改造的复合威胁，这可能进一步威胁该区域此前未被发现的隐存多样性（cryptic diversity）。