Does divergent selection predict the evolution of mate preference and reproductive isolation in the tropical butterfly genus Melinaea (Nymphalidae: Ithomiini)?

Abstract

Many studies have shown that speciation can be facilitated when a trait under divergent selection also causes assortative mating. In Müllerian mimetic butterflies, a change in wing colour pattern can cause reproductive isolation. However, colour pattern divergence does not always lead to reproductive isolation. Understanding how divergent selection affects speciation requires identifying the mechanisms that promote mate preference and/or choosiness. This study addresses whether shifts in wing colour pattern drives mate preference and reproductive isolation in the tropical butterfly genus Melinaea (Nymphalidae: Ithomiini), and focuses on five taxa that form a speciation continuum, from subspecies to fully recognized species. Using genetic markers, wing colour pattern quantification, male pheromone characterization and behavioural assays of mating preference, we characterize the extent of genetic and phenotypic differentiation between taxa and compare it to the level of reproductive isolation. We show strong premating isolation between the closely related species M. satevis and M. marsaeus, in addition to genetic and phenotypic (colour pattern and pheromones) differentiation. By contrast, M. menophilus and M. marsaeus consist of pairs of subspecies that differ for colour pattern but that cannot be differentiated genetically. Pheromonal differentiation of subspecies was significant only for M. marsaeus, although most individuals were indistinguishable. Melinaea menophilus and M. marsaeus also differ in the strength of assortative mating, suggesting that mate preference has evolved only in M. marsaeus, consistent with selection against maladaptive offspring, as subspecific ‘hybrids’ of M. marsaeus have intermediate, non‐mimetic colour patterns, unlike those of M. menophilus which display either parental phenotypes. We conclude that a shift in colour pattern per se is not sufficient for reproductive isolation, but rather, the evolution of assortative mating may be caused by selection against maladaptive intermediate phenotypes. This study suggests that mate preference and assortative mating evolve when adaptive, and that even in the early stages of divergence, reproductive isolation can be nearly complete due to mating preferences.

Renewed diversification following Miocene landscape turnover in a Neotropical butterfly radiation

“…We found a strong dampening of local speciation in the Central (Hill et al, 2012;Jiggins et al, 2006;McClure & Elias, 2016McClure et al 2019). Contrasting with those clades, four other Amazonian radiations showed diversification rates decreasing through time, meaning that diversification was highest immediately after the retreat of the Pebas.…”

“…Drivers of diversification in the core group probably include radiation on Solanaceae (Willmott & Freitas, ), which were already diverse in the Neotropics during the Miocene (Dupin et al, ), in conjunction with a diversity of habitats along the slopes of the Andes. Speciation was also potentially mediated by shifts in mimicry patterns (Chazot et al, ; Willmott & Mallet, ), which can generate reproductive isolation in mimetic butterflies (Jiggins, Naisbit, Coe, & Mallet, ), including Ithomiini (Jiggins et al, ; McClure et al ). Those ecological drivers of diversification were probably at play both in the Andes and in non‐Andean areas, after the Pebas retreat.…”

“…Three Amazonian radiations, the genus Melinaea (which comprises the rapidly diversifying Melinaea group) and the clade Mechanitis + Forbestra in the backbone and the Brevioleria group in the core group showed increasing speciation rates towards the present. Those radiations may be interpreted as supporting an effect of recent climatic fluctuations during the Pleistocene on the diversification of the Melinaea group (and the Mechanitis + Forbestra clade), although ecological drivers of speciation classically invoked in mimetic butterfly diversification, such as colour pattern and host‐plant shifts, cannot be ruled out (Hill et al, ; Jiggins et al, ; McClure & Elias, , ; McClure et al ). Contrasting with those clades, four other Amazonian radiations showed diversification rates decreasing through time, meaning that diversification was highest immediately after the retreat of the Pebas.…”

3-Acetoxy-fatty acid isoprenyl esters from androconia of the ithomiine butterfly Ithomia salapia

“…Despite the geographic overlap in distribution, a recent genetic study showed limited gene flow [4]. Reproductive isolation in mimetic butterflies can be driven by multiple factors, notably non-random mating based on color pattern and/or sexual pheromones [6][7][8]. Determining whether the closely related subspecies of I. salapia differ in the chemical composition of volatiles is, therefore, of great interest.…”

Contrasting genomic and phenotypic outcomes of hybridization between pairs of mimetic butterfly taxa across a suture zone

“…Wing colour pattern is known to cause pre‐ and post‐zygotic reproductive isolation in Müllerian mimetic butterflies (e.g., Chamberlain, Hill, Kapan, Gilbert, & Kronforst, 2009; Jiggins et al, 2001; Mallet & Barton, 1989; Merrill et al, 2011; Merrill et al, 2012; Naisbit, Jiggins, Linares, Salazar, & Mallet, 2002), including Ithomiini (McClure et al, 2019).…”