Polymorphic Butterfly Reveals the Missing Link in Ecological Speciation

Abstract

Ecological speciation occurs when ecologically-based divergent selection causes the evolution of reproductive isolation. While there are many empirical examples of this process, there exists a poorly characterized stage during which the traits that distinguish species ecologically and reproductively segregate in a single population. Using a combination of genetic mapping, mate choice experiments, field observations, and population genetics, we studied a butterfly population with a mimetic wing color polymorphism and found that they exhibited partial color-based assortative mate preference. These traits represent the divergent, ecologically-based signal and preference components of sexual isolation that usually distinguish incipient and sibling species. The association between behavior and recognition trait in a single population may enhance the probability of speciation and provides an example for the missing link between an interbreeding population and isolated species.Research focused on a variety of biological systems has yielded compelling examples of ecological speciation (1, Table S1). Some of the specific traits that have diverged due to natural selection and cause reproductive isolation as a result include host choice in phytophagous insects such as Rhagoletis flies (2) and Timema walking-sticks (3), body size in stickleback fish (4), coloration in cichlid fish (5) and poison-dart frogs (6,7), and flowering time (8) and pollinator (9) in plants. While previous work on ecological speciation has been instrumental in characterizing the direct link between natural selection and speciation (10,11), it has largely focused on systems in which populations are highly differentiated (Table S1). However, the means by which interbreeding populations transition to assortative mating on the basis of a trait under divergent natural selection are generally unknown.Mimetic wing patterns in Heliconius butterflies provide a clear example of a trait involved in ecological speciation (12). Heliconius butterflies are chemically defended and warninglycolored. Their evolutionary history has been marked by widespread color pattern divergence among closely-related species and geographic subpopulations (13). This is combined with convergence among distantly-related species as a result of natural selection for Müllerian mimicry (13), or mimicry among mutually protected species. Furthermore, closely-related

Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures

“…Overall, 88% of females reject their own morph more often than dissimilar ones. The genetics of mate preference are unknown in this species, but male preference loci causing assortative mating have been mapped in other Heliconius species and shown to be linked to color patterning loci, such as K and optix (10,31,32). Moreover, in the Heliconius cydno-melpomene clade, the Yb color locus, a homolog to the wing-patterning supergene of H. numata, was associated with female mate preference (33).…”

“…However, polymorphism is sometimes found within populations of warningly colored species (10)(11)(12)(13). One spectacular example is the mimetic polymorphism found in the Amazonian butterfly Heliconius numata.…”

Diversification of the cold-adapted butterfly genus Oeneis related to Holarctic biogeography and climatic niche shifts

“…A clade is rarely the pure product of allopatry (Muller and Beharegaray, 2010;Imada et al, 2011). Geographical speciation can be coupled with ecological speciation (Hall, 2005;Willmott et al, 2001;Matos-Maravi et al, 2013) involving the differentiation of species lineages by changes in habitat use or behaviour (Jiggins, 2008;Chamberlain et al, 2009). Diversification along climatic gradients, such as moisture (Rieseberg et al, 1999;Gee, 2004) or temperature (Keller and Seehausen, 2012) has been documented in several clades.…”

Pairing dynamics and the origin of species

“…A principal cost of assortative mating results from the reduced number of mating encounters experienced by rare morphs, thus constraining the evolution of assortative mating in models of speciation with gene flow [2,5,7,8,11 -16]. Yet, assortative mating at the species level is so strong and ubiquitous in nature that our ignorance of its place during the evolutionary sequence between interbreeding populations and reproductively isolated species has been referred to as the 'missing link' in evolution [17].…”