Abstract
Homoploid hybrid speciation is the formation of a new hybrid species without change in chromosome number. So far, there has been a lack of direct molecular evidence for hybridization generating novel traits directly involved in animal speciation. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has been proposed as a hybrid species, and its color pattern can be recreated by introgression of the H. m. melpomene red band into the genetic background of the yellow banded H. cydno cordula. This hybrid color pattern is also involved in mate choice and leads to reproductive isolation between H. heurippa and its close relatives. Here, we provide molecular evidence for adaptive introgression by sequencing genes across the Heliconius red band locus and comparing them to unlinked wing patterning genes in H. melpomene, H. cydno, and H. heurippa. 670 SNPs distributed among 29 unlinked coding genes (25,847bp) showed H. heurippa was related to H. c. cordula or the three species were intermixed. In contrast, among 344 SNPs distributed among 13 genes in the red band region (18,629bp), most showed H. heurippa related with H. c. cordula, but a block of around 6,5kb located in the 3′ of a putative kinesin gene grouped H. heurippa with H. m. melpomene, supporting the hybrid introgression hypothesis. Genealogical reconstruction showed that this introgression occurred after divergence of the parental species, perhaps around 0.43Mya. Expression of the kinesin gene is spatially restricted to the distal region of the forewing, suggesting a mechanism for pattern regulation. This gene therefore constitutes the first molecular evidence for adaptive introgression during hybrid speciation and is the first clear candidate for a Heliconius wing patterning locus.
Highlights
Identifying the genetic mechanisms involved in speciation is an important challenge in the study of evolution [1,2,3]
Among 344 single nucleotide polymorphism (SNP) distributed among 13 genes in the red band region (18,629bp), most showed H. heurippa related with H. c. cordula, but a block of around 6,5kb located in the 39 of a putative kinesin gene grouped H. heurippa with H. m. melpomene, supporting the hybrid introgression hypothesis
We sampled molecular markers both linked to the locus controlling red color pattern and across the genome of Heliconius heurippa and its putative parents, H. cydno and H. melpomene
Summary
Identifying the genetic mechanisms involved in speciation is an important challenge in the study of evolution [1,2,3]. Empirical studies have shown that species differences can be localized in just a few genomic regions [3,4,5], and that reproductive isolation is more achieved when traits causing assortative mating are subject to natural selection [6,7] Such characteristics have been termed ‘magic traits’ [6] and can facilitate speciation as a side-effect of ecological divergence in the presence of ongoing gene flow [8,9]. The two scenarios contrast in their genomic signature, with hybrid trait speciation potentially involving introgression of just a few adaptively important loci into the genetic background of one of the parental species, making it much more difficult to detect using traditional approaches based on ‘neutral markers’ [21] This is in addition to the fact that detecting hybrid speciation at the molecular level is difficult anyway, due to incomplete linage sorting and historical gene flow, which can leave similar signatures of shared variation [24]
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