Tempo and timing of ecological trait divergence in bird speciation

Abstract

Organismal traits may evolve either gradually or in rapid pulses, but the relative importance of these modes in the generation of species differences is unclear. Additionally, while pulsed evolution is frequently assumed to be associated with speciation events, few studies have explicitly examined how the tempo of trait divergence varies with respect to different geographical phases of speciation, starting with geographic isolation and ending, in many cases, with spatial overlap (sympatry). Here we address these issues by combining divergence time estimates, trait measurements and geographic range data for 952 avian sister species pairs worldwide to examine the tempo and timing of trait divergence in recent speciation events. We show that patterns of divergence in key ecological traits are not gradual, but instead seem to follow a pattern of relative stasis interspersed with evolutionary pulses of varying magnitude. We also find evidence that evolutionary pulses generally precede sympatry, and that greater trait disparity is associated with sympatry. These findings suggest that early pulses of trait divergence promote subsequent transitions to sympatry, rather than occurring after sympatry has been established. Incorporating models with evolutionary pulses of varying magnitude into speciation theory may explain why some species pairs achieve rapid sympatry whereas others undergo prolonged geographical exclusion.

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Fig. 1: The speciation cycle and phenotypic trait divergence.
Fig. 2: Tempo of body mass divergence for avian sister species.
Fig. 3: Timing of body mass divergence pulses and sympatry.
Fig. 4: Phylogenetic patterns of contact and sympatry across avian sister species.
Fig. 5: Factors associated with the establishment of secondary contact and sympatry in birds.

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Acknowledgements

We are grateful to numerous data collectors who contributed to eBird, GenBank and the CRC bird body mass dataset (see Supplementary Information). We also thank N. Alioravainen, E. Braun, S. Jones, R. Kimball, D. Ksepka, M. Neate-Clegg, A. Pigot, A. Ragsdale and G. Zhelezov for data collection and technical assistance. This work was supported by the National Science Foundation (DEB-1208428 to J.G.B.), the Natural Environment Research Council (NE/I028068/1 to J.A.T.) and the Oxford Clarendon Fund and US–UK Fulbright Commission (to C.S.).

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J.G.B. and J.P.M. conceived the study; J.G.B., J.P.M. and J.A.T. designed the conceptual framework and analyses; J.G.B. performed dating analyses and assembled phylogenetic, occurrence and body mass information; J.A.T. and C.S. provided morphometric data; J.P.M. integrated datasets, and designed and performed statistical analyses with significant input from J.G.B., J.A.T. and C.S.; J.P.M. and C.S. produced figures and tables; J.P.M. wrote the manuscript, with significant input from all authors.

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Correspondence to Jay P. McEntee.

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Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figures, Supplementary Tables and Supplementary Code

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Supplementary Data 1-8

Supplementary Data 1: Sister pair dataset used for analysis of the probability of contact, and of breeding contact, by divergence time. Supplementary Data 2: Sister pair dataset used for GLM designed to find predictors associated with contact and breeding contact. Supplementary Data 3: Sister pairs in contact, used for GLM designed to find predictors associated with sympatry given contact. Supplementary Data 4: Morphological measurements by species. Supplementary Data 5: Log body mass divergence by species pair, used for analyses of body mass divergence tempo and mode. Supplementary Data 6: Species pairs from Burleigh et al. 2015 phylogeny excluded from co-occurrence analyses, with reasons for exlcusion. Supplementary Data 7: Fossil calibrations. Supplementary Data 8: Metadata for all specimens and wild-caught birds used for morphological measurements of the beak and wing. Specimens are listed alphabetically by species. A forthcoming database publication led by J.A.T. will include morphological measurements by specimen

Supplementary Table 9

Multi-model inference of predictor effects for sympatry versus parapatry of bird sister species in contact

Supplementary Table 11

Sensitivity analyses investigating predictor effects for contact versus absence of contact in bird sister species, from an alternate approach to phylogenetic inference and divergence time estimation

Supplementary Table 13

Sensitivity analyses investigating predictor effects for sympatry versus parapatry of bird sister species in contact, from an alternate approach to phylogenetic inference and divergence time estimation

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McEntee, J.P., Tobias, J.A., Sheard, C. et al. Tempo and timing of ecological trait divergence in bird speciation. Nat Ecol Evol 2, 1120–1127 (2018). https://doi.org/10.1038/s41559-018-0570-y

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