Incorporating the full annual cycle when studying reproductive isolation and speciation

Abstract

As individual tracking devices and year-round genetic sampling become more accessible, research on the historically understudied nonbreeding period has exploded in the past decade. These studies are revealing tremendous inter- and intraspecific variation in migratory, molting, and other nonbreeding strategies, thereby informing efforts to protect bird populations throughout the entire annual cycle. However, we still have much to learn about where and when nonbreeding adaptive variation influences reproductive isolation and speciation. Previous work has demonstrated that some adaptations to conditions in different nonbreeding areas or migratory routes can fuel diversification by precluding opportunities for diverging lineages to interbreed or, in instances where lineages do interbreed, manifesting as disadvantageous phenotypes in hybrids. In this paper, we provide an overview of both established and speculative processes through which the primary nonbreeding events in the avian annual cycle (i.e. molt, migration, and overwintering) may interact to regulate gene flow between avian lineages. Although the relatively few but well-described examples of divergence in nonbreeding phenotypes contributing to reproductive isolation suggest nonbreeding divergence is a common mode of speciation in birds, a growing number of population genetic studies reporting nonbreeding divergence in the absence of reproductive isolation seemingly suggest the opposite conclusion. We outline processes that could result in this apparent contradiction and propose general comparative frameworks to test factors that may predictably mediate the relationship between nonbreeding divergence and reproductive isolation. In the past, a shortage of nonbreeding natural history and population genetic data have impeded our ability to test these predictions in more than just a few systems. We urge evolutionary biologists to pay closer attention to conservation-oriented studies, which are rapidly filling these knowledge gaps and presenting opportunities to better understand the true role of nonbreeding divergence in avian diversification.