Historical demography of Mullerian mimicry in the neotropical Heliconius butterflies

Abstract

We compare the historical demographies of two Müllerian comimetic butterfly species: Heliconius erato and Heliconius melpomene. These species show an extensive parallel geographic divergence in their aposematic wing phenotypes. Recent studies suggest that this coincident mosaic results from simultaneous demographic processes shaped by extrinsic forces over Pleistocene climate fluctuations. However, DNA sequence variation at two rapidly evolving unlinked nuclear loci, Mannose phosphate isomerase (Mpi) and Triose phosphate isomerase (Tpi), show that the comimetic species have quite different quaternary demographies. In H. erato, despite ongoing lineage sorting across the Andes, nuclear genealogical estimates showed little geographical structure, suggesting high historical gene flow. Coalescent-based demographic analysis revealed population growth since the Pliocene period. Although these patterns suggest vicariant population subdivision associated with the Andean orogeny, they are not consistent with hypotheses of Pleistocene population fragmentation facilitating allopatric wing phenotype radiation in H. erato. In contrast, nuclear genetic diversity, theta, in H. melpomene was reduced relative to its comimic and revealed three phylogeographical clades. The pattern of coalescent events within regional clades was most consistent with population growth in relatively isolated populations after a recent period of restricted population size. These different demographic histories suggest that the wing-pattern radiations were not coincident in the two species. Instead, larger effective population size (N(e)) in H. erato, together with profound population change in H. melpomene, supports an earlier hypothesis that H. erato diversified first as the model species of this remarkable mimetic association.

Fig. 1.

ML genealogies for H. erato and H. melpomene of Tpi (A) and Mpi (B) alleles. The following models of evolution were the best: TrN+I+G, P(I) = 0.3402, a = 0.8850, for Tpi H. erato; TrN+I, P(I) = 0.6301, for Tpi H. melpomene; GTR+G, a = 0.6013, for Mpi H. erato; and TrN+I, P(I) = 0.4376, for Mpi H. melpomene. MP genealogies were qualitatively and quantitatively similar. Numbers on the branches are parsimony bootstrap values for the equivalent nodes on the ML tree. Sequences are labeled with a racial code, individual number, allele identity (A or B), and country code (see Table 3 for additional information on phylogenetic analysis). The three main geographic regions are indicated by bars. Racial identity for H. erato is given as follows: CHE, H. erato chestertonii; CYR, H. erato cyrbia; EMM, H. erato emma; ERA, H. erato erato; ETY, H. erato etylus; FAV, H. erato favorinus; HYD, H. erato hydara; LAT, H. erato latavitta; NOT, H. erato notabilis; PET, H. erato petiverana; and HIM, H. himera. Racial identity for H. melpomene is given as follows: AGLA, H. melpomene aglaope; MALL, H. melpomene malleti; AMAR, H. melpomene amaryllis; CYTH, H. melpomene cythera; ECUA, H. melpomene ecuadoriensis; MELP, H. melpomene melpomene; PLES, H. melpomene plessini; ROSI, H. melpomene rosina; and THEL, H. melpomene thelxiopeia. Pe, Peru; EcW, Ecuador, western slope of Andes; EcE, Ecuador, eastern slope of Andes; Pa, Panama; Co, Colombia; TT, Trinidad and Tobago; FG, French Guyana. In B, H. melpomene alleles marked with an asterisk are hypothesized to be of hybrid origin based a larger sampling of alleles (V. Bull, M. Beltrán, E. Bermingham, C. Jiggins, W.O.M., and J. Mallet, unpublished data).

Fig. 2.

Estimated demographic histories of the H. erato and H. melpomene radiations, for Tpi (A) and Mpi (B). The thicker, piecewise plots are the generalized skyline plots. The approximate timescale assumes an evolutionary rate of ≈1.1–1.2% per lineage per 1 million years (1). Thus, the approximate Pleistocene–Pliocene boundary corresponds to a genetic distance of ≈0.023 substitutions per site. The thinner, smooth curves represent the parametric ML demographic history (see Table 2). Plots for H. erato (green) and H. melpomene (blue) are shown on the same graph.