Phylogenetic Discordance at the Species Boundary: Comparative Gene Genealogies Among Rapidly Radiating Heliconius Butterflies

Abstract

Recent adaptive radiations provide excellent model systems for understanding speciation, but rapid diversification can cause problems for phylogenetic inference. Here we use gene genealogies to investigate the phylogeny of recent speciation in the heliconiine butterflies. We sequenced three gene regions, intron 3 ( approximately 550 bp) of sex-linked triose-phosphate isomerase (Tpi), intron 3 ( approximately 450 bp) of autosomal mannose-phosphate isomerase (Mpi), and 1,603 bp of mitochondrial cytochrome oxidase subunits I and II (COI and COII), for 37 individuals from 25 species of Heliconius and related genera. The nuclear intron sequences evolved at rates similar to those of mitochondrial coding sequences, but the phylogenetic utility of introns was restricted to closely related geographic populations and species due to high levels of indel variation. For two sister species pairs, Heliconius erato-Heliconius himera and Heliconius melpomene-Heliconius cydno, there was highly significant discordance between the three genes. At mtDNA and Tpi, the hypotheses of reciprocal monophyly and paraphyly of at least one species with respect to its sister could not be distinguished. In contrast alleles sampled from the third locus, Mpi, showed polyphyletic relationships between both species pairs. In all cases, recent coalescence of mtDNA lineages within species suggests that polyphyly of nuclear genes is not unexpected. In addition, very similar alleles were shared between melpomene and cydno, implying recent gene flow. Our finding of discordant genealogies between genes is consistent with models of adaptive speciation with ongoing gene flow and highlights the need for multiple locus comparisons to resolve phylogeny among closely related species.

Searching for candidate speciation genes using a proteomic approach: seminal proteins in field crickets

“…R. Soc. B (2008) introgression (Rieseberg et al 1999;Beltran et al 2002;Machado & Hey 2003;Ting et al 2000;Panithanarak et al 2004;Dopman et al 2005;Payseur & Nachman 2005). These studies, which represent genome scans or scans of the sex chromosome, have also defined genome regions that show little evidence of introgression or for which closely related species are exclusive groups (Machado & Hey 2003;Panithanarak et al 2004;Dopman et al 2005).…”

Historical demography of Müllerian mimicry in the neotropical Heliconius butterflies

“…Although these sister-species pairs are known to hybridize in the wild at low (H. cydno and H. melpomene) to moderate (H. himera and H. erato) levels, significant behavioral, ecological, and genetic differentiation warrant species-level designation (15)(16)(17). Nonetheless, the exact phylogenetic relationships remain problematic (1). We also sampled the following outgroup species: Heliconius clysonimus, Heliconius telesiphe, and Heliconius hecale (see Table 3).…”

“…DNA sequence data were obtained from Mpi and Tpi according to Beltrán et al (1). For each individual, 3-10 clones were sequenced to identify distinct alleles.…”

“…These distantly related (1,2), unpalatable species have both radiated into almost 30 wing phenotypic races. However, in any one location across their sympatric ranges, they exhibit nearly perfect convergence in their warningly colored wing patterns.…”

The Hunting of the SNaRC: A Snarky Solution to the Species Problem

“…Named species can be formed by repeated speciation (Turner 2002) or by hybridization between other species (Bogart 2003;Rieseberg 1997). Or particular species may have an incomplete coalescence of genetic lineages or haplotypes (Beltrán, Jiggins, et al 2002;Després, Pettex, et al 2002).…”