Genomic divergence in allopatric Northern Cardinals of the North American warm deserts is linked to behavioral differentiation.

Kaiya L Provost,William M Mauck,Brian Tilston Smith

doi:10.1002/ece3.4596

Kaiya L Provost, William M Mauck + Show 1 more

Open Access

https://doi.org/10.1002/ece3.4596

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Abstract

Biogeographic barriers are considered important in initiating speciation through geographic isolation, but they rarely indiscriminately and completely reduce gene flow across entire communities. Explicitly demonstrating which factors are associated with gene‐flow levels across barriers would help elucidate how speciation is initiated and isolation maintained. Here, we investigated the association of behavioral isolation on population differentiation in Northern Cardinals (Cardinalis cardinalis) distributed across the Cochise Filter Barrier, a region of transitional habitat which separates the Sonoran and Chihuahuan deserts of North America. Using genomewide markers, we modeled demographic history by fitting the data to isolation and isolation‐with‐migration models. The best‐fit model indicated that desert populations diverged in the Pleistocene with low, historic, and asymmetric gene flow across the barrier. We then tested behavioral isolation using reciprocal call‐broadcast experiments to compare song recognition between deserts, controlling for song dialect changes within deserts. We found that male Northern Cardinals in both deserts were most aggressive to local songs and failed to recognize across‐barrier songs. A correlation of genomic differentiation and strong song discrimination is consistent with a model where speciation is initiated across a barrier and maintained by behavioral isolation.

Highlights

Populations are frequently separated by biogeographic barriers, the ecological and physical features in the landscape that prevent organ‐ isms with particular traits from dispersing across them (Coyne & Orr, 2004; Mayr, 1963; Simpson, 1940)
We found that the Northern Cardinal had low gene flow and strong male song discrimination across the Cochise Filter Barrier
We showed that song discrimination between deserts is greater than song discrimination within deserts, indicating that these birds ex‐ hibit divergence in song beyond what would be expected through dialect changes alone

Summary

| INTRODUCTION

Populations are frequently separated by biogeographic barriers, the ecological and physical features in the landscape that prevent organ‐ isms with particular traits from dispersing across them (Coyne & Orr, 2004; Mayr, 1963; Simpson, 1940). For populations distributed across the Cochise Filter Barrier, it is unclear which mechanisms have fa‐ cilitated or inhibited gene flow To address one such mechanism by which barriers may prevent gene flow after isolation, we examined the role of behavior in a resident songbird, the Northern Cardinal (Cardinalis cardinalis). Northern Cardinal males are generally less aggressive in response to unfamiliar songs, and the species is sensitive to dialect changes that can occur over tens of kilometers, responding with decreased levels of aggression to more distant di‐ alects (Anderson & Conner, 1985; Lemon, 1966, 1974). By combining genomic es‐ timates of isolation and introgression with responses of wild birds to song differences involved in mate choice, we explored whether behavioral isolation helps regulate gene flow across filter barriers

| MATERIALS AND METHODS

| DISCUSSION

Findings

CONFLICT OF INTEREST