Explosive Cenozoic origin and diversity-dependent diversification dynamics shaped the evolution of Australian skipper butterflies

Australia was predominantly tropical for most of the early Cenozoic, then transitioned to a cooler and drier climate in the Oligocene. In response to this increasing aridity, some lineages adapted to more xeric ecosystems, contracted, or became restricted to increasingly fragmented mesic refugia, or went extinct. Yet, the lack of macroevolutionary studies at a continental scale precludes a better understanding of Australian biodiversity patterns and processes during the Cenozoic. Here, we infer a robust dated phylogenomic tree for a radiation of Australian endemic butterflies, the Trapezitinae skippers, to test the impact of biotic and abiotic drivers on Cenozoic diversification dynamics in Australia. These butterflies originated during the Eocene (ca. 42 Ma) in the mesic biome of Australia. Trapezitinae exploded in diversity during a cool, dry period in the late Oligocene and early Miocene, then experienced a sharp deceleration in speciation. Xeric ecosystems appear to have been colonized more recently, supporting the hypothesis of arid and semi-arid biomes as evolutionary sinks. Temperature-dependent and phytophagy-dependent diversification models received little support. Instead, we find evidence for diversity-dependent processes with a declining diversification in Trapezitinae likely linked to limited ecological opportunities following a rapid initial burst of diversification.

新生代早期的澳大利亚绝大多数区域均处于热带气候格局，随后在渐新世时期逐步向温凉干燥的气候转型。为应对持续加剧的干旱化进程，部分演化支逐渐适应了旱生生态系统，种群分布范围收缩，或被局限于愈发碎片化的湿润避难所中，乃至最终走向灭绝。然而，当前缺乏大陆尺度的宏观演化研究，这极大限制了我们对新生代时期澳大利亚生物多样性模式与演化过程的深入认知。
本研究针对澳大利亚特有蝴蝶类群——梯弄蝶亚科（Trapezitinae skippers）的辐射演化类群，构建了可靠的定年系统发育基因组学树，以此检验生物与非生物驱动因子对澳大利亚新生代物种多样化动态的影响。该类蝴蝶起源于始新世（约4200万年前）的澳大利亚湿润生物群区。梯弄蝶亚科的物种多样性在渐新世晚期至中新世早期的温凉干燥时期出现爆发式增长，随后物种形成速率急剧放缓。
研究发现，旱生生态系统的殖民事件发生时间相对较晚，这为“干旱与半干旱生物群区属于演化汇”的假说提供了支持。依赖温度与植食性的物种多样化模型未获得有力证据支撑。与之相反，本研究找到了支持多样性依赖过程的证据：梯弄蝶亚科的多样化速率随时间推移逐渐下降，这很可能与物种快速初始爆发后生态位机会受限存在关联。