Neural divergence and hybrid disruption between ecologically isolatedHeliconiusbutterflies

Abstract

The importance of behavioral evolution during speciation is well established, but we know little about how this is manifest in sensory and neural systems. A handful of studies have linked specific neural changes to divergence in host or mate preferences associated with speciation. However, the degree to which brains are adapted to local environmental conditions, and whether this contributes to reproductive isolation between close relatives that have diverged in ecology, remains unknown. Here, we examine divergence in brain morphology and neural gene expression between closely related, but ecologically distinct, Heliconius butterflies. Despite ongoing gene flow, sympatric species pairs within the melpomene–cydno complex are consistently separated across a gradient of open to closed forest and decreasing light intensity. By generating quantitative neuroanatomical data for 107 butterflies, we show that Heliconius melpomene and Heliconius cydno clades have substantial shifts in brain morphology across their geographic range, with divergent structures clustered in the visual system. These neuroanatomical differences are mirrored by extensive divergence in neural gene expression. Differences in both neural morphology and gene expression are heritable, exceed expected rates of neutral divergence, and result in intermediate traits in first-generation hybrid offspring. Strong evidence of divergent selection implies local adaptation to distinct selective optima in each parental microhabitat, suggesting the intermediate traits of hybrids are poorly matched to either condition. Neural traits may therefore contribute to coincident barriers to gene flow, thereby helping to facilitate speciation.

Urbanization extends flight phenology and leads to local adaptation of seasonal plasticity in Lepidoptera

“…As we made sure to only include sites so that urban–rural distances were short (10 to 40 km), our evidence for differences appears remarkable, especially for P. napi given its considerably higher mobility, and hence higher gene flow, than C. clathrata ( 42 , 50 ). However, heritable divergence in the face of ongoing gene flow is achievable when a strong selection pressure leads to divergent selection and local adaptation to distinct selective optima, and indeed, divergence between populations in the face of gene flow is considered strong evidence for local adaptation ( 51 , 52 ). Since the diapause trait is essential for winter survival in temperate and boreal insects, it is under strong selection, which could counteract such gene flow ( 53 , 54 ).…”

Light environment influences mating behaviours during the early stages of divergence in tropical butterflies

“…Unlike other examples [39,40,49], the effects we see here act across very short time and spatial scales, reflecting the fluctuating sensory conditions experienced by our study species in their rainforest environments. By contrast to more divergent Heliconius species pairs [50,51], H. heurippa and H. t. linaresi are not known to differ in ecology or habitat type, and there is little reason to suspect that differences in their sensory environment drive divergence in mating preferences, or sensory behaviours more broadly. Instead, differences in female wing pattern (driven by local selection for aposematism) likely impose divergent sexual selection on male preferences to improve their ability to find receptive females [16].…”

A brain-wide analysis maps structural evolution to distinct anatomical modules

“…Previous studies examining how the brain evolves have largely been restricted to comparative studies between closely related, albeit different species, and these studies have revealed gross differences in neuroanatomy, connectivity, and function between derived animals (5, 9, 10, 12, 14). However, the Astyanax model provides a powerful tool for assessing how the brain evolves in a single species with multiple divergent forms and an extant ancestor (20, 22, 37).…”