Simpson's fossil-record inspired model of ‘adaptive zones’ proposes that evolution is dominated by small fluctuations within adaptive zones, occasionally punctuated by larger shifts between zones. This model can help explain why the process of population divergence often results in weak or moderate reproductive isolation (RI), rather than strong RI and distinct species. Applied to the speciation process, the adaptive zones hypothesis makes two inter-related predictions: (i) large shifts between zones are relatively rare, (ii) when large shifts do occur they generate stronger RI than shifts within zones. Here, we use ecological, phylogenetic and behavioural data to test these predictions in Timema stick insects. We show that host use in Timema is dominated by moderate shifts within the systematic divisions of flowering plants and conifers, with only a few extreme shifts between these divisions. However, when extreme shifts occur, they generate greater RI than do more moderate shifts. Our results support the adaptive zones model, and suggest that the net contribution of ecological shifts to diversification is dependent on both their magnitude and frequency. We discuss the generality of our findings in the light of emerging evidence from diverse taxa that the evolution of RI is not always the only factor determining the origin of species diversity.

This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

辛普森受化石记录启发的“适应区”模型提出，进化主要由适应区内的小波动主导，偶尔会被区域之间的较大变化所打断。该模型可以帮助解释为什么种群分化过程通常会导致弱或中度的生殖隔离 (RI)，而不是强 RI 和不同的物种。应用于物种形成过程，适应性区域假设做出两个相互关联的预测：(i) 区域之间的大转变相对罕见，(ii) 当大转变确实发生时，它们产生的 RI 比区域内的转变更强。在这里，我们使用生态、系统发育和行为数据来测试这些对Timema竹节虫的预测。我们展示了Timema中的主机使用主要是开花植物和针叶树系统分部内的适度变化，这些分部之间只有少数极端变化。然而，当极端转变发生时，它们比更温和的转变产生更大的 RI。我们的结果支持适应区模型，并表明生态变化对多样化的净贡献取决于它们的幅度和频率。我们根据来自不同分类群的新证据讨论了我们发现的一般性，即 RI 的进化并不总是决定物种多样性起源的唯一因素。

这篇文章是主题问题“走向物种形成的完成：超越第一道障碍的生殖隔离的进化”的一部分。