The phoenix hypothesis of speciation

Genetic divergence among allopatric populations builds reproductive
isolation over time. This process is accelerated when populations face a
changing environment, but abrupt change also places populations at risk of
extinction. Here we use simulations of Fisher’s geometric model with
explicit population dynamics to explore the genetic changes that occur in
the face of environmental changes. We show that evolutionary rescue leads
to the fixation of mutations whose effects are larger on average and that
these mutations are more likely to lead to reproductive isolation,
compared with populations not at risk of extinction. We refer to the
formation of new species from the ashes of populations in decline as the
phoenix hypothesis of speciation. The phoenix hypothesis predicts more
substantial hybrid fitness breakdown among populations surviving a higher
extinction risk. The hypothesis was supported when many loci underlie
adaptation. When, however, there was only a small number of potential
rescue mutations, we found that mutations fixed in different populations
were more likely to be identical, with parallel changes reducing
isolation. With a limited genomic potential for adaptation, we find
support for a modified version of the phoenix hypothesis where
reproductive isolation builds fastest in populations subject to an
intermediate extinction risk.

异域种群间的遗传分化随时间推移逐步积累生殖隔离。当种群遭遇环境变化时，该过程会被加速，但环境骤变也会将种群置于灭绝风险之中。本研究借助搭载显式种群动力学的费希尔几何模型（Fisher’s geometric model）开展模拟实验，以此探究环境变化背景下发生的遗传改变。研究结果显示，相较于未面临灭绝风险的种群，进化拯救会使得平均效应更大的突变得以固定，且此类突变更易引发生殖隔离。我们将从衰退种群的“灰烬”中孕育新物种的过程，命名为物种形成的凤凰假说（phoenix hypothesis of speciation）。该假说预测，在更高灭绝风险下存活的种群间，杂种适合度衰退会更为显著。当适应过程涉及众多基因座时，该假说得到了实证支持。然而，当潜在拯救突变的数量较少时，我们发现不同种群中固定的突变更易趋于一致，平行突变会削弱生殖隔离的形成。在基因组适应潜力有限的情境下，本研究支持修正版的凤凰假说：即生殖隔离的积累速度在处于中等灭绝风险的种群中最快。