Ecological and genetic factors influencing the transition between host‐use strategies in sympatric Heliconius butterflies

Abstract

Shifts in host-plant use by phytophagous insects have played a central role in their diversification. Evolving host-use strategies will reflect a trade-off between selection pressures. The ecological niche of herbivorous insects is partitioned along several dimensions, and if populations remain in contact, recombination will break down associations between relevant loci. As such, genetic architecture can profoundly affect the coordinated divergence of traits and subsequently the ability to exploit novel habitats. The closely related species Heliconius cydno and H. melpomene differ in mimetic colour pattern, habitat and host-plant use. We investigate the selection pressures and genetic basis underlying host-use differences in these two species. Hostplant surveys reveal that H. melpomene specializes on a single species of Passiflora. This is also true for the majority of other Heliconius species in secondary growth forest at our study site, as expected under a model of interspecific competition. In contrast, H. cydno, which uses closed-forest habitats where both Heliconius and Passiflora are less common, appears not to be restricted by competition and uses a broad selection of the available Passiflora. However, other selection pressures are likely involved, and field experiments reveal that early larval survival of both butterfly species is highest on Passiflora menispermifolia, but most markedly so for H. melpomene, the specialist on that host. Finally, we demonstrate an association between host-plant acceptance and colour pattern amongst interspecific hybrids, suggesting that major loci underlying these important ecological traits are physically linked in the genome. Together, our results reveal ecological and genetic associations between shifts in habitat, host use and mimetic colour pattern that have likely facilitated both speciation and coexistence.

Butterfly Learning and the Diversification of Plant Leaf Shape

“…The ability to learn to associate new leaf shapes with oviposition sites may allow females to tailor their search image to the local Passiflora community. Specifically, in the case of H. erato, there are three important host species in the Gamboa area which have dramatically different leaf shapes, P. biflora, P. auriculata, and P. coriaceae (Merrill et al, 2013). Furthermore, there is considerable variation in all three species both between individuals and between young and old leaves.…”

Multilocus Species Trees Show the Recent Adaptive Radiation of the Mimetic Heliconius Butterflies

“…S7, available on Dryad at http://dx.doi.org/10.5061/dryad.44b4j). This is despite extensive evidence for at least three species (H. melpomene, H. cydno, and H. timareta), if not the currently recognized five (also including H. pachinus and H. heurippa): premating behavioral isolation (Merrill et al 2011), host plant usage and habitat preference (Benson et al 1975;Brown 1981;Merrill et al 2013), morphology (Penz 1999), and genome-wide genetic structure Arias et al 2014). The small number of nucleotide differences between the biological species is consistent with interspecific gene flow, which led to a reduction in differentiation across the genome.…”

“…All Heliconius are found in broadly similar Neotropical habitats (Brown 1981) and most of the species appear to originate on the eastern slope of the Central and North Andes (Rosser et al 2012). Heliconius is far more diverse than the other nine genera of the tribe, and individual species show high disparity in their dietary adaptations (Benson et al 1975;Merrill et al 2013), and wing pattern diversity (Brown 1981;Jiggins 2008). Numerous field and laboratory experiments have demonstrated the adaptive value of wing patterns in protection from predators (Langham 2004).…”

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

“…2011b), host plant choice (Merrill et al. 2013), pollen load, and microhabitat (Estrada and Jiggins 2002). Hybrid color pattern phenotypes are attacked more frequently than parental forms, indicating disruptive selection against hybrids (Merrill et al.…”