Neuroanatomical shifts mirror patterns of ecological divergence in three diverse clades of mimetic butterflies

Benito Wainwright, Stephen H Montgomery

Research output: Contribution to journalArticle (Academic Journal)peer-review

11 Citations (Scopus)
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Abstract

Microhabitat partitioning in heterogenous environments can support more diverse communities but may expose partitioned species to distinct perceptual challenges. Divergence across microhabitats could therefore lead to local adaptation to contrasting sensory conditions across small spatial scales, but this aspect of community structuring is rarely explored. Diverse communities of ithomiine butterflies provide an example where closely related species partition tropical forests, where shifts in mimetic coloration are tightly associated with shifts in habitat preference. We test the hypothesis that these mimetic and ecological shifts are associated with distinct patterns of sensory neural investment by comparing brain structure across 164 individuals of 16 species from three ithomiine clades. We find distinct brain morphologies between Oleriina and Hypothyris, which are mimetically homogenous and occupy a single microhabitat. Oleriina, which occurs in low-light microhabitats, invests less in visual brain regions than Hypothyris, with one notable exception, Hyposcada anchiala, the only Oleriina sampled to have converged on mimicry rings found in Hypothyris. We also find that Napeogenes, which has diversified into a range of mimicry rings, shows intermediate patterns of sensory investment. We identify flight height as a critical factor shaping neuroanatomical diversity, with species that fly higher in the canopy investing more in visual structures. Our work suggests that the sensory ecology of species may be impacted by, and interact with, the ways in which communities of closely related organisms are adaptively assembled.
Original languageEnglish
Pages (from-to)1806-1820
Number of pages15
JournalEvolution
Volume76
Issue number8
DOIs
Publication statusPublished - 2022

Bibliographical note

Funding Information:
We are thankful to Á. Barragán, E. Moreno, P. Jarrín, and D. Lasso from the Estación Científica Yasuní, Pontificia Universidad Católica del Ecuador, and M. Arévalo from the Parque Nacional Yasuní Ministerio del Ambiente for assisting with collection and export permits. We are also grateful to F. Ramirez Castro for his assistance in the field in 2011. Many thanks also to K. Jepson and colleagues at the University of Bristol's Wolfson Bioimaging facility for confocal microscope support and to M. Elias and N. Chazot for giving permission to use their flight height data and phylogenetic tree. We also thank S. England, D. Rivas Sanchez and members of the EBAB group for insightful comments on a draft manuscript. This work was funded by a Royal Commission for the Exhibition Research Fellowship, a Royal Society Small Grant (RG110466) and an NERC IRF (NE/N014936/1) to SHM, and a GW4+ NERC DTP to JBW.

Funding Information:
We are thankful to Á. Barragán, E. Moreno, P. Jarrín, and D. Lasso from the Estación Científica Yasuní, Pontificia Universidad Católica del Ecuador, and M. Arévalo from the Parque Nacional Yasuní Ministerio del Ambiente for assisting with collection and export permits. We are also grateful to F. Ramirez Castro for his assistance in the field in 2011. Many thanks also to K. Jepson and colleagues at the University of Bristol's Wolfson Bioimaging facility for confocal microscope support and to M. Elias and N. Chazot for giving permission to use their flight height data and phylogenetic tree. We also thank S. England, D. Rivas Sanchez and members of the EBAB group for insightful comments on a draft manuscript. This work was funded by a Royal Commission for the Exhibition Research Fellowship, a Royal Society Small Grant (RG110466) and an NERC IRF (NE/N014936/1) to SHM, and a GW4+ NERC DTP to JBW.

Publisher Copyright:
© 2022 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.

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