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Estimating the relative fitness of local adaptive peaks: the aerodynamic costs of flight in mimetic passion-vine butterflies Heliconius

ABSTRACT: In a related paper, we demonstrated that mimetic Heliconius butterflies have converged in wing-beat frequency and degree of asymmetry in the wing motion, whereas sister species are dissimilar in these same traits. Warning signals of sympatric, distasteful species converge in evolutionary models in order to educate their predators more efficiently that the signal is associated with unprofitable prey. Barring other constraints, the behaviours of the different co-mimetic pairs should ultimately converge on that behaviour which minimizes the energetic cost of flight. We estimated the energetic cost of each mimic's flight behaviour in order to predict the difference in height of each fitness peak and the direction of convergent selection qualitatively. Following adjustments for body mass, mimetic Heliconius melpomene and Heliconius erato required more aerodynamic power than Heliconius cydno and Heliconius sapho. This difference was attributed to the slower flight speeds and higher wing-beat frequencies of H. melpomene and H. erato. Consequently, H. melpomene and H. erato expended more energy per unit distance per unit body mass than H. cydno and H. sapho. However, differences in body mass may equalize energy budgets and stabilize the sympatric coexistence of the two pairs of co-mimics.

SUBMITTER: Srygley R

PROVIDER: S-EPMC1690455 | biostudies-literature | 1999 Nov

REPOSITORIES: biostudies-literature

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Project description:The unpalatable and warning-patterned butterflies Heliconius erato and Heliconius melpomene provide the best studied example of mutualistic Müllerian mimicry, thought-but rarely demonstrated-to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of H. erato and H. melpomene, and this was initially hailed as one of the most striking known cases of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of H. erato and H. melpomene, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of H. erato and H. melpomene. Cophylogenetic historical reconstructions support repeated codivergence of mimetic populations, from the base of the sampled radiations. Pairwise distance correlation tests, based on our coalescent analyses plus recently published AFLP and wing colour pattern gene data, also suggest that the phylogenies of H. erato and H. melpomene show significant topological congruence. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of H. erato and H. melpomene occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. Our results suggest that differences in within-species genetic divergence are the result of a greater overall effective population size for H. erato relative to H. melpomene and do not imply incongruence in the timing of their phylogenetic radiations. Repeated codivergence between Müllerian co-mimics, predicted to exert mutual selection pressures, strongly suggests coevolution. Our results therefore support a history of reciprocal coevolution between Müllerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change.

Project description:Müllerian mimicry among Neotropical Heliconiini butterflies is an excellent example of natural selection, associated with the diversification of a large continental-scale radiation. Some of the processes driving the evolution of mimicry rings are likely to generate incongruent phylogenetic signals across the assemblage, and thus pose a challenge for systematics. We use a data set of 22 mitochondrial and nuclear markers from 92% of species in the tribe, obtained by Sanger sequencing and de novo assembly of short read data, to re-examine the phylogeny of Heliconiini with both supermatrix and multispecies coalescent approaches, characterize the patterns of conflicting signal, and compare the performance of various methodological approaches to reflect the heterogeneity across the data. Despite the large extent of reticulate signal and strong conflict between markers, nearly identical topologies are consistently recovered by most of the analyses, although the supermatrix approach failed to reflect the underlying variation in the history of individual loci. However, the supermatrix represents a useful approximation where multiple rare species represented by short sequences can be incorporated easily. The first comprehensive, time-calibrated phylogeny of this group is used to test the hypotheses of a diversification rate increase driven by the dramatic environmental changes in the Neotropics over the past 23 myr, or changes caused by diversity-dependent effects on the rate of diversification. We find that the rate of diversification has increased on the branch leading to the presently most species-rich genus Heliconius, but the change occurred gradually and cannot be unequivocally attributed to a specific environmental driver. Our study provides comprehensive comparison of philosophically distinct species tree reconstruction methods and provides insights into the diversification of an important insect radiation in the most biodiverse region of the planet.

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Estimating the relative fitness of local adaptive peaks: the aerodynamic costs of flight in mimetic passion-vine butterflies Heliconius

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