RESUMO
When populations experience different sensory conditions, natural selection may favor sensory system divergence, affecting peripheral structures and/or downstream neural pathways. We characterized the outer eye morphology of sympatric Heliconius butterflies from different forest types and their first-generation reciprocal hybrids to test for adaptive visual system divergence and hybrid disruption. In Panama, Heliconius cydno occurs in closed forests, whereas Heliconius melpomene resides at the forest edge. Among wild individuals, H. cydno has larger eyes than H. melpomene, and there are heritable, habitat-associated differences in the visual brain structures that exceed neutral divergence expectations. Notably, hybrids have intermediate neural phenotypes, suggesting disruption. To test for similar effects in the visual periphery, we reared both species and their hybrids in common garden conditions. We confirm that H. cydno has larger eyes and provide new evidence that this is driven by selection. Hybrid eye morphology is more H. melpomene-like despite body size being intermediate, contrasting with neural trait intermediacy. Overall, our results suggest that eye morphology differences between H. cydno and H. melpomene are adaptive and that hybrids may suffer fitness costs due to a mismatch between the peripheral visual structures and previously described neural traits that could affect visual performance.
Assuntos
Borboletas , Seleção Genética , Simpatria , Animais , Borboletas/anatomia & histologia , Borboletas/genética , Borboletas/fisiologia , Olho/anatomia & histologia , Panamá , Feminino , Masculino , Hibridização GenéticaRESUMO
Locating food in heterogeneous environments is a core survival challenge. The distribution of resources shapes foraging strategies, imposing demands on perception, learning and memory, and associated brain structures. Indeed, selection for foraging efficiency is linked to brain expansion in diverse taxa, from primates1 to Hymenopterans2. Among butterflies, Heliconius have a unique dietary adaptation, actively collecting and feeding on pollen, providing a source of essential amino acids as adults, negating reproductive senescence and facilitating an extended longevity3. Several lines of evidence suggest that Heliconius learn the spatial location of pollen resources within an individual's home range4, and spatial learning may be more pronounced at these large spatial scales. However, experimental evidence of spatial learning in Heliconius, or any other butterfly, is so far absent. We therefore tested the ability of Heliconius to learn the spatial location of food rewards at three ecologically-relevant spatial scales, representing multiple flowers on a single plant, multiple plants within a locality, and multiple localities. Heliconius were able to learn spatial information at all three scales, consistent with this ability being an important component of their natural foraging behaviour.
Assuntos
Borboletas , Animais , Memória Espacial , Dieta , Pólen , AlimentosRESUMO
Insects may acquire social information by active communication and through inadvertent social cues. In a foraging setting, the latter may indicate the presence and quality of resources. Although social learning in foraging contexts is prevalent in eusocial species, this behaviour has been hypothesized to also exist between conspecifics in non-social species with sophisticated behaviours, including Heliconius butterflies. Heliconius are the only butterfly genus with active pollen feeding, a dietary innovation associated with a specialized, spatially faithful foraging behaviour known as trap-lining. Long-standing hypotheses suggest that Heliconius may acquire trap-line information by following experienced individuals. Indeed, Heliconius often aggregate in social roosts, which could act as 'information centres', and present conspecific following behaviour, enhancing opportunities for social learning. Here, we provide a direct test of social learning ability in Heliconius using an associative learning task in which naive individuals completed a colour preference test in the presence of demonstrators trained to feed randomly or with a strong colour preference. We found no evidence that Heliconius erato, which roost socially, used social information in this task. Combined with existing field studies, our results add to data which contradict the hypothesized role of social learning in Heliconius foraging behaviour.
Assuntos
Borboletas , Aprendizado Social , Humanos , Animais , Aprendizagem , Comportamento Animal , DietaRESUMO
Despite insertions and deletions being the most common structural variants (SVs) found across genomes, not much is known about how much these SVs vary within populations and between closely related species, nor their significance in evolution. To address these questions, we characterized the evolution of indel SVs using genome assemblies of three closely related Heliconius butterfly species. Over the relatively short evolutionary timescales investigated, up to 18.0% of the genome was composed of indels between two haplotypes of an individual Heliconius charithonia butterfly and up to 62.7% included lineage-specific SVs between the genomes of the most distant species (11 Mya). Lineage-specific sequences were mostly characterized as transposable elements (TEs) inserted at random throughout the genome and their overall distribution was similarly affected by linked selection as single nucleotide substitutions. Using chromatin accessibility profiles (i.e., ATAC-seq) of head tissue in caterpillars to identify sequences with potential cis-regulatory function, we found that out of the 31,066 identified differences in chromatin accessibility between species, 30.4% were within lineage-specific SVs and 9.4% were characterized as TE insertions. These TE insertions were localized closer to gene transcription start sites than expected at random and were enriched for sites with significant resemblance to several transcription factor binding sites with known function in neuron development in Drosophila We also identified 24 TE insertions with head-specific chromatin accessibility. Our results show high rates of structural genome evolution that were previously overlooked in comparative genomic studies and suggest a high potential for structural variation to serve as raw material for adaptive evolution.
Assuntos
Borboletas , Animais , Borboletas/genética , Cromatina/genética , Elementos de DNA Transponíveis/genética , Genômica , Mutação INDEL , Drosophila/genética , Evolução MolecularRESUMO
Microhabitat choice plays a major role in shaping local patterns of biodiversity. In butterflies, stratification in flight height has an important role in maintaining community diversity. Despite its presumed importance, the role of behavioural shifts in early stages of speciation in response to differences in habitat structure is yet to be established. Here, we investigated variation in flight height behaviour in two closely related Heliconius species, H. erato cyrbia and H. himera, which produce viable hybrids but are isolated across an environmental gradient, spanning lowland wet forest to high-altitude scrub forest. Speciation in this pair is associated with strong assortative mating, but ecological isolation and local adaptation are also considered essential for complete reproductive isolation. We quantified differences in flight height and forest structure across the environmental gradient and tested the importance of resource distribution in explaining flight behaviour. We then used common garden experiments to test whether differences in flight height reflect individual responses to resource distribution or genetically determined shifts in foraging behaviour. We found that the two species fly at different heights in the wild, and demonstrated that this can be explained by differences in the vertical distribution of plant resources. In both the wild and captivity, H. himera choose to fly lower and feed at lower positions, closely mirroring differences in resource availability in the wild. Given expectations that foraging efficiency contributes to survival and reproductive success, we suggest that foraging behaviour may reflect local adaptation to divergent forest structures. Our results highlight the potential role of habitat-dependent divergence in behaviour during the early stages of speciation.
La elección de microhábitat juega un papel determinante en los patrones locales de biodiversidad. En las mariposas, la estratificación (entendida como altura de vuelo) cumple un rol importante al promover la diversidad de las comunidades. A pesar de esta asumida importancia, todavía está por establecerse el rol de los cambios comportamentales en estadios tempranos de especiación en respuesta a diferencias en la estructura del hábitat. Aquí investigamos la variación en el comportamiento de estratificación en dos especies de mariposas Heliconius cercanamente emparentadas: H. erato cyribia y H. himera, las cuales producen híbridos viables, pero están aisladas a lo largo de un gradiente ambiental que va desde el bosque húmedo tropical de tierras bajas hasta el bosque de matorrales de altitud. La especiación en esta pareja de mariposas está asociada con un alto grado de emparejamiento selectivo, pero el aislamiento ecológico y la adaptación local también son considerados esenciales para un aislamiento reproductivo completo. Mostramos que las dos especies vuelan a alturas distintas, y demostramos que esto se explica por diferencias en la distribución vertical de los recursos florísticos. Posteriormente, usando experimentos controlados de jardín, exploramos si esta divergencia en altura de vuelo está determinada ambientalmente. Tanto en la naturaleza como en cautividad, H. himera escoge volar más bajo y alimentarse en lugares más bajos, lo que es consistente con las diferencias en la disponibilidad de recursos en la naturaleza. Dada la expectativa de que la eficiencia en el forrajeo contribuye al éxito reproductivo y de supervivencia, sugerimos que el comportamiento de forrajeo podría reflejar adaptación local a estructuras de bosque divergentes. Nuestros resultados resaltan el potencial rol de la divergencia dependiente del hábitat en el comportamiento en estadios tempranos de especiación.