Anatomy of a neotropical insect radiation

Background: Much evolutionary theory predicts that diversity arises via both adaptive radiation (diversification driven by selection against niche-overlap within communities) and divergence of geographically isolated populations. We focus on tropical fruit flies (Blepharoneura, Tephritidae) that reveal unexpected patterns of niche-overlap within local communities. Throughout the Neotropics, multiple sympatric non-interbreeding populations often share the same highly specialized patterns of host use (e.g., flies are specialists on flowers of a single gender of a single species of host plants). Lineage through time (LTT) plots can help distinguish patterns of diversification consistent with ecologically limited adaptive radiation from those predicted by ecologically neutral theories. Here, we use a time-calibrated phylogeny of Blepharoneura to test the hypothesis that patterns of Blepharoneura diversification are consistent with an “ecologically neutral” model of diversification that predicts that diversification is primarily a function of time and space.
Results: The Blepharoneura phylogeny showed more cladogenic divergence associated with geography than with shifts in host-use. Shifts in host-use were associated with ~20% of recent splits (<3 Ma), but >60% of older splits (>3 Ma). In the overall tree, gamma statistic and maximum likelihood model fitting showed no evidence of diversification rate changes though there was a weak signature of slowing diversification rate in one of the component clades.
Conclusions: Overall patterns of Blepharoneura diversity are inconsistent with a traditional explanation of adaptive radiation involving decreases in diversification rates associated with niche-overlap. Sister lineages usually use the same host-species and host-parts, and multiple non-interbreeding sympatric populations regularly co-occur on the same hosts. We suggest that most lineage origins (phylogenetic splits) occur in allopatry, usually without shifts in host-use, and that subsequent dispersal results in assembly of communities composed of multiple sympatric non-interbreeding populations of flies that share the same hosts.

背景：诸多演化理论均指出，生物多样性的产生同时经由两种途径：一是适应辐射（adaptive radiation，即由群落内部针对生态位重叠的选择压力所驱动的物种分化），二是地理隔离种群的分化。本研究聚焦热带实蝇类群——折翅实蝇属（Blepharoneura，实蝇科Tephritidae），该类群展现出局地群落中存在意料之外的生态位重叠模式。在整个新热带区，多个同域生殖隔离种群往往共享高度特化的寄主利用模式，例如，该实蝇仅特化寄生于单一寄主植物物种的单性花器官。类群-时间（Lineage Through Time, LTT）图可用于区分两类物种分化模式：一类符合生态受限的适应辐射，另一类则由生态中性理论所预测。本研究利用折翅实蝇属的时间校准系统发育树，检验如下假说：折翅实蝇属的物种分化模式符合“生态中性”分化模型，该模型预测物种分化主要是时间与空间的函数。
结果：折翅实蝇属的系统发育树显示，与寄主利用转变相关的分支分化程度，远低于与地理分化相关的分支分化程度。寄主利用转变与约20%的近期分化事件（距今<3百万年）相关，但与超过60%的古老分化事件（距今>3百万年）相关。对整体系统发育树的伽马统计量与最大似然模型拟合结果显示，未发现多样化速率发生改变的证据；不过其中一个分支类群呈现出微弱的多样化速率放缓信号。
结论：折翅实蝇属的整体多样性模式，与传统的适应辐射解释并不一致——该传统理论认为，多样化速率会随生态位重叠加剧而下降。姊妹支系通常共享相同的寄主物种与寄主部位，且多个生殖隔离的同域种群常共同出现于相同寄主之上。我们认为，绝大多数支系起源（系统发育分化事件）均发生于异域成种过程中，且通常未伴随寄主利用的转变；后续的扩散导致群落构建，形成由多个共享相同寄主的同域生殖隔离实蝇种群组成的群落。