Cultural evolution may accelerate population divergence and speciation, though most support for this hypothesis is restricted to scenarios of allopatric speciation driven by random cultural drift. By contrast, the role of cultural evolution in non-allopatric speciation (i.e. speciation with gene flow) has received much less attention. One clade in which cultural evolution may have figured prominently in speciation with gene flow includes the conifer-seed-eating finches in the red crossbill (Loxia curvirostra) complex. Here we focus on Cassia crossbills (Loxia sinesciuris; an ecotype recently split taxonomically from red crossbills) that learn social contact calls from their parents. Previous work found that individuals modify their calls throughout life such that they become increasingly divergent from a closely related, sympatric red crossbill ecotype. This open-ended modification of calls could lead to character displacement if it causes population-level divergence in call structure that, in turn, reduces (maladaptive) heterospecific flocking. Heterospecific flocking is maladaptive because crossbills use public information from flockmates to assess resource quality, and feeding rates are depressed when flockmates differ in their ability to exploit a shared resource (i.e. when flockmates are heterospecifics). We confirm the predictions of character displacement by documenting substantial population-level divergence in Cassia crossbill call structure over just two decades and by using field experiments to demonstrate that Cassia and red crossbills differentially respond to these evolved differences in call structure, reducing heterospecific flock formation. Moreover, because crossbills choose mates from within flocks, a reduction in heterospecific flocking should increase assortative mating and may have been critical for speciation of Cassia crossbills in the face of ongoing gene flow in as few as 5000 years. Our results provide evidence for a largely neglected yet potentially widespread mechanism by which reproductive isolation can evolve between sympatric lineages as a byproduct of adaptive cultural evolution.
Keywords: character displacement; crossbills; cultural evolution; public information; reproductive isolation; speciation.
Conflict of interest statement
We declare we have no competing interests.
Assortative flocking in crossbills and implications for ecological speciation.Proc Biol Sci. 2012 Oct 22;279(1745):4223-9. doi: 10.1098/rspb.2012.1500. Epub 2012 Aug 22. Proc Biol Sci. 2012. PMID: 22915674 Free PMC article.
Patterns of genetic variation in the adaptive radiation of New World crossbills (Aves: Loxia).Mol Ecol. 2006 Jun;15(7):1873-87. doi: 10.1111/j.1365-294X.2006.02895.x. Mol Ecol. 2006. PMID: 16689904
A coevolutionary arms race causes ecological speciation in crossbills.Am Nat. 2007 Apr;169(4):455-65. doi: 10.1086/511961. Am Nat. 2007. PMID: 17273981
Patterns of coevolution in the adaptive radiation of crossbills.Ann N Y Acad Sci. 2010 Sep;1206:1-16. doi: 10.1111/j.1749-6632.2010.05702.x. Ann N Y Acad Sci. 2010. PMID: 20860680 Review.
Character displacement: ecological and reproductive responses to a common evolutionary problem.Q Rev Biol. 2009 Sep;84(3):253-76. doi: 10.1086/605079. Q Rev Biol. 2009. PMID: 19764283 Free PMC article. Review.