Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies

Abstract

Ecological speciation proceeds through the accumulation of divergent traits that contribute to reproductive isolation, but in the face of gene flow traits that characterize incipient species may become disassociated through recombination. Heliconius butterflies are well known for bright mimetic warning patterns that are also used in mate recognition and cause both pre- and post-mating isolation between divergent taxa. Sympatric sister taxa representing the final stages of speciation, such as Heliconius cydno and Heliconius melpomene, also differ in ecology and hybrid fertility. We examine mate preference and sterility among offspring of crosses between these species and demonstrate the clustering of Mendelian colour pattern loci and behavioural loci that contribute to reproductive isolation. In particular, male preference for red patterns is associated with the locus responsible for the red forewing band. Two further colour pattern loci are associated, respectively, with female mating outcome and hybrid sterility. This genetic architecture in which 'speciation genes' are clustered in the genome can facilitate two controversial models of speciation, namely divergence in the face of gene flow and hybrid speciation.

Figure 1.

Male mate preference of H. cydno, H. melpomene and their hybrids. Proportion of courtship events directed towards live H. melpomene females by (a) H. cydno (white bars) and H. melpomene (red bars) males; (b) their F₁ hybrid males; and male offspring from backcross broods to each species; (c) backcross to H. melpomene and (d) backcross to H. cydno. In each case, red bars represent individuals with a red forewing bar (BB or Bb) and white bars individuals without the red forewing bar (bb).

Figure 2.

Male mate preference is associated with forewing colour. The probability of courting H. melpomene live females (a) and wing pattern models (b) by backcross hybrids to H. cydno (BC) that have the red forewing band (Bb, red squares) and those that do not (bb, white squares), where 1 would indicate a complete preference for H. melpomene and 0 a preference for H. cydno. Blacked-out males had their forewing colour pattern obscured in order to prevent self-matching. Dashed lines represent the probabilities of courting live H. melpomene females for H. melpomene (MP) and H. cydno (CP) males. Support limits are asymptotically equivalent to 95% confidence intervals and were obtained by searching for values that decreased ln(L) by two units.

Figure 3.

Female mate choice is associated with the hindwing Yb colour pattern locus. Data are counts of female offspring from backcross to H. cydno broods (BC) differing at the Yb locus that mated with H. cydno (white), H. melpomene (red) or did not mate (black) within 3 days of introduction to an experimental cage containing 20 males of each species.

Figure 4.

Failure to oviposit is associated with the Ac forewing colour pattern locus. White bars represent female offspring from backcross to H. cydno broods (BC) that are homozygous at the locus (acac) for the H. cydno allele and black bars represent heterozygous females at the locus (Acac), having inherited an allele from both H. cydno and H. melpomene. Data are counts of females that failed to lay eggs.