Allochronic and geographic reproductive isolation in an African songbird
Kim G. Mortega • J. Carlos Illera • Mariëlle L. van Toor • Beate Apfelbeck • Paul Johnson • Jason Matthiopoulos • Deborah A. Dawson • Terry Burke • B. Rosemary Grant • Barbara Helm
Ecological speciation – the divergence by local adaptation to different environments – and the role of geographic isolation for population divergence have been studied extensively. In contrast, allochronic isolation – the separation of populations by timing – remains mostly unconsidered when studying speciation. Populations might exhibit temporal barriers to gene flow, because seasonal activities must be accurately timed to avoid mismatches with the environment, which can have severe fitness consequences. The evolution of rigid reproductive schedules, endogenously generated biological rhythms, buffers organisms from responding to misleading, unpredictable variability of environments. The Afrotropical songbird, Saxicola torquata (African stonechat), is a well-studied species with robust reproductive schedules. We studied genetic, song, and morphological divergence between populations of S. torquata with asynchronous breeding onsets, and populations separated by geographic barriers. We modeled the environmental connectivity between populations to quantify the relative contributions of timing and geography to reproductive isolation. We found that allochronic and geographic populations are genetically differentiated as judged from microsatellite loci and mitochondrial DNA. This genetic structure is strongly concordant with patterns of song and morphology divergence of S. torquata. Populations are spatially connected with no geographic or environmental barriers to gene flow, which strongly indicates population divergence as the result of allochronic isolation. Furthermore, S. torquata females prefer mates with synchronized reproductive timing, thus promoting reproductive barriers by behavioral isolation. Our results indicate that the evolutionary dynamics of allochronic isolation and the ecological forces that shape them may be key drivers for population divergence and ultimately speciation.