Abstract
The role of environmental gradients in speciation remains contentious. Theory suggests speciation without geographic isolation is plausible if divergent natural selection is strong enough to counteract gene flow, but empirical examples are elusive. Tropical mountains provide strong and temporally stable environmental gradients that can promote local adaptation and population genetic structure. Pairs of closely related species with adjacent but divergent elevational ranges are common in these environments, a pattern that suggests parapatric speciation (i.e. speciation with moderate gene flow), but have rarely been studied in a speciation genomics framework. Here we use genomic data from modern and historical museum specimens to provide evidence for speciation with gene flow across an elevational gradient in a pair of New Guinea kingfishers. We find that the lowland species Syma torotoro and montane species S. megarhyncha form discrete genotypic clusters with bimodal variance in phenotypic traits. Despite this, demographic inference, D-statistics, and phylogenetic networks indicate range-wide gene flow over long time periods, with divergence concentrated in small regions of the genome shaped by positive selection. We propose these data can be explained by a “magic trait” model of ecological speciation where selection on body size also affects mate choice. Our results provide a rare validation of theoretical models of adaptive speciation and are consistent with a strong influence of tropical thermal stability on diversification. We suggest the primary role of selection across elevational gradients is the maintenance of species boundaries in the face of incomplete reproductive isolation, a mechanism for generating high tropical biodiversity.
Significance Speciation without geographic isolation can occur across environmental gradients when disruptive natural selection reduces effective migration between locally adapted populations. Theory suggests this process is widely plausible in a range of circumstances, but empirical examples remain rare. Strong and temporally stable thermal stratification in tropical mountains can select for narrow thermal tolerances and reduce dispersal across elevations, potentially promoting this process and contributing to globally high levels of biodiversity in these environments. We provide multiple lines of evidence for speciation across an elevational gradient in a pair of New Guinea kingfisher species that segregate by elevation, maintain species limits in the face of high levels of long-term gene flow across their range, and differ primarily in small regions of the genome shaped by positive selection. These results indicate selection across elevational gradients can maintain species boundaries in the face of incomplete reproductive isolation, a mechanism generating high tropical biodiversity.
