Punctuated evolution in the learned songs of African sunbirds.

Jay P Mcentee,Rauri C K Bowie,Joshua V Peñalba,Gleb Zhelezov,Lyubov Chumakova,Sylvester Karimi,J Gordon Burleigh,Maneno Mbilinyi,Nadje Najar,Elia Mulungu,Chacha Werema

doi:10.1098/rspb.2021.2062

Abstract

Learned traits are thought to be subject to different evolutionary dynamics than other phenotypes, but their evolutionary tempo and mode has received little attention. Learned bird song has been thought to be subject to rapid and constant evolution. However, we know little about the evolutionary modes of learned song divergence over long timescales. Here, we provide evidence that aspects of the territorial songs of Eastern Afromontane sky island sunbirds Cinnyris evolve in a punctuated fashion, with periods of stasis of the order of hundreds of thousands of years or more, broken up by evolutionary pulses. Stasis in learned songs is inconsistent with learned traits being subject to constant or frequent change, as would be expected if selection does not constrain song phenotypes over evolutionary timescales. Learned song may instead follow a process resembling peak shifts on adaptive landscapes. While much research has focused on the potential for rapid evolution in bird song, our results suggest that selection can tightly constrain the evolution of learned songs over long timescales. More broadly, these results demonstrate that some aspects of highly variable, plastic traits can exhibit punctuated evolution, with stasis over long time periods.

Highlights

Signal evolution has long been thought to be important to the process of animal speciation [1], in part because many closely related species have distinct signals while differing little in other traits [2,3]
While much research has focused on the potential for rapid evolution in bird song, our results suggest that selection can tightly constrain the evolution of learned songs over long timescales
Previous work has suggested that stabilizing selection on learned traits should be inadequate to prevent the divergence of genetic predispositions by drift, facilitating more rapid divergence in those genes underlying traits [12]

Summary

Background

Signal evolution has long been thought to be important to the process of animal speciation [1], in part because many closely related species have distinct signals while differing little in other traits [2,3]. If rapid cultural evolution serves as a first step in further divergence that includes underlying genetic change, learned songs may diverge gradually over time, and potentially at high rates. The strongest empirical evidence for the evolutionary trajectory of learned song relevant to speciation likely comes from studies of the greenish warbler Phylloscopus trochiloides, which exhibits nearly continuous variation across geographical space, suggestive of gradual evolution [20]. It remains possible that learned song can exhibit punctuated evolution, where pulses of divergence occur against a backdrop of stasis, or highly bounded, nonaccumulating evolution Such a pattern may arise if innate song-learning predispositions remain fixed for long periods of time, with infrequent pulses of evolutionary change. This question has rarely been posed for signalling phenotypes [27]

Results

Discussion

Conclusion