16 research outputs found
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Adaptation to altitude in Heliconius butterflies
Local adaptation is an important process for studying recent evolutionary change. The environment changes drastically along steep clines, such as mountains, and diverse sets of challenges are predicted to drive local adaptation. Thus, these clines represent ideal settings to identify the traits and genomic mechanisms that allow some organisms to succeed across wide geographical ranges, which is a major goal of evolutionary biology. In this thesis I explore the environmental variables, phenotypic traits, and genomics underlying adaptation to altitude in the Heliconius butterfly genus.
Firstly, using a collection of over 3500 wings I discovered that wing morphology varies predictably across elevations, with species and populations in the highlands having rounder wings than those in the lowlands. This study also highlighted that life-history, whether larvae are gregarious or solitary, determines the direction of wing sexual size dimorphism across species. Secondly, to understand the microclimates experienced in the wild by Heliconius butterflies, I measured hourly temperature and humidity for a full year in 28 sites across elevations and microhabitats on both sides of the Andes. The canopy greatly buffered the climate within the forest, but publicly available datasets failed to accurately predict these temperatures. Further, I found that species inhabiting higher altitudes were less tolerant to heat in the wild, while common-garden reared individuals of H. melpomene were equally tolerant after one generation, showing plasticity for this trait. Thirdly, with a dataset of over 600 whole-genome sequenced H. erato and H. melpomene individuals from four elevational clines, I found many parallel signatures of local adaptation to high altitude across clines and sides of the Andes, especially within H. erato. Finally, I studied the genomic basis of one of the traits I identified as being potentially involved in adaptation to altitude, wing shape. By combining common-garden rearing of highland and lowland populations of H. erato and H. melpomene and 666 whole-genome sequences from a published study, I found that wing aspect ratio is highly heritable, and identified relevant candidates for future functional studies.
Overall, this work highlights that butterflies readily adapt to their local environment and that they do so in a more convergent fashion than previously thought. This thesis lays the groundwork for an exciting new branch of study for Heliconius research, where we combine the long fascination for their natural history and speciation, with new approaches to study how they adapt to the environment.University of Cambridge Earth System Science NERC Doctoral Training Partnershi
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Altitude and life-history shape the evolution of Heliconius wings.
Phenotypic divergence between closely related species has long interested biologists. Taxa that inhabit a range of environments and have diverse natural histories can help understand how selection drives phenotypic divergence. In butterflies, wing color patterns have been extensively studied but diversity in wing shape and size is less well understood. Here, we assess the relative importance of phylogenetic relatedness, natural history, and habitat on shaping wing morphology in a large dataset of over 3500 individuals, representing 13 Heliconius species from across the Neotropics. We find that both larval and adult behavioral ecology correlate with patterns of wing sexual dimorphism and adult size. Species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera, where females are larger. Species in the pupal-mating clade are smaller than those in the adult-mating clade. Interestingly, we find that high-altitude species tend to have rounder wings and, in one of the two major Heliconius clades, are also bigger than their lowland relatives. Furthermore, within two widespread species, we find that high-altitude populations also have rounder wings. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing coloration
Riparian reserves protect butterfly communities in selectively logged tropical forest
Selective logging is the most widespread habitat disturbance in tropical forests. Primary forest set-asides along riparian zones are mandated in many countries and a key question is whether these riparian reserves provide biodiversity conservation benefits. We characterise butterfly communities in fixed-width riparian reserves of 30 m on each bank along narrow streams (<10 m) paired with interior logged forest transects, and in primary forests within a selective logging concession in the south-western Brazilian Amazon. We found that primary forest species richness was more similar to riparian reserves than to paired interior logged forest points, whereas abundance remained higher in both riparian reserves and interior logged points, likely due to the intrusion of canopy-dwelling species in disturbed habitats, as previously reported in the literature. Butterfly assemblages within riparian reserves were more similar to unlogged primary forests than interior logged points, and canopy height in riparian reserves was associated with increased assemblage similarity to primary forest points. Changes in abundance relative to primary forest were of a larger magnitude in interior logged points than in riparian reserves within logged forests, highlighting the role of riparian reserves in maintaining primary forest-like communities. We found no particular primary forest butterfly clades to be more sensitive to changes in abundance than other clades. Synthesis and applications. Mandatory conservation set-asides around streams or rivers (riparian buffers) have an important role in protecting the abundance and composition of primary forest butterfly assemblages within selective logging concessions in tropical rainforests. This study highlights the need to assess the conservation value of protecting unlogged riparian forest strips in other taxa to inform policy
Evolutionary and ecological processes influencing chemical defense variation in an aposematic and mimetic Heliconius butterfly
Chemical defences against predators underlie the evolution of aposematic coloration and mimicry, which are classic examples of adaptive evolution. Surprisingly little is known about the roles of ecological and evolutionary processes maintaining defence variation, and how they may feedback to shape the evolutionary dynamics of species. Cyanogenic Heliconius butterflies exhibit diverse warning color patterns and mimicry, thus providing a useful framework for investigating these questions. We studied intraspecific variation in de novo biosynthesized cyanogenic toxicity and its potential ecological and evolutionary sources in wild populations of Heliconius erato along environmental gradients, in common-garden broods and with feeding treatments. Our results demonstrate substantial intraspecific variation, including detectable variation among broods reared in a common garden. The latter estimate suggests considerable evolutionary potential in this trait, although predicting the response to selection is likely complicated due to the observed skewed distribution of toxicity values and the signatures of maternal contributions to the inheritance of toxicity. Larval diet contributed little to toxicity variation. Furthermore, toxicity profiles were similar along steep rainfall and altitudinal gradients, providing little evidence for these factors explaining variation in biosynthesized toxicity in natural populations. In contrast, there were striking differences in the chemical profiles of H. erato from geographically distant populations, implying potential local adaptation in the acquisition mechanisms and levels of defensive compounds. The results highlight the extensive variation and potential for adaptive evolution in defense traits for aposematic and mimetic species, which may contribute to the high diversity often found in these systems.Peer reviewe
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Genomics of altitude-associated wing shape in two tropical butterflies.
Understanding how organisms adapt to their local environment is central to evolution. With new whole-genome sequencing technologies and the explosion of data, deciphering the genomic basis of complex traits that are ecologically relevant is becoming increasingly feasible. Here, we studied the genomic basis of wing shape in two Neotropical butterflies that inhabit large geographical ranges. Heliconius butterflies at high elevations have been shown to generally have rounder wings than those in the lowlands. We reared over 1,100 butterflies from 71 broods of H. erato and H. melpomene in common-garden conditions and showed that wing aspect ratio, that is, elongatedness, is highly heritable in both species and that elevation-associated wing aspect ratio differences are maintained. Genome-wide associations with a published data set of 666 whole genomes from across a hybrid zone, uncovered a highly polygenic basis to wing aspect ratio variation in the wild. We identified several genes that have roles in wing morphogenesis or wing aspect ratio variation in Drosophila flies, making them promising candidates for future studies. There was little evidence for molecular parallelism in the two species, with only one shared candidate gene, nor for a role of the four known colour pattern loci, except for optix in H. erato. Thus, we present the first insights into the heritability and genomic basis of within-species wing aspect ratio in two Heliconius species, adding to a growing body of evidence that polygenic adaptation may underlie many ecologically relevant traits
Cortex cis -regulatory switches establish scale colour identity and pattern diversity in Heliconius
In Heliconius butterflies, wing colour pattern diversity and scale types are controlled by a few genes of large effect that regulate colour pattern switches between morphs and species across a large mimetic radiation. One of these genes, cortex, has been repeatedly associated with colour pattern evolution in butterflies. Here we carried out CRISPR knockouts in multiple Heliconius species and show that cortex is a major determinant of scale cell identity. Chromatin accessibility profiling and introgression scans identified cis-regulatory regions associated with discrete phenotypic switches. CRISPR perturbation of these regions in black hindwing genotypes recreated a yellow bar, revealing their spatially limited activity. In the H. melpomene/timareta lineage, the candidate CRE from yellow-barred phenotype morphs is interrupted by a transposable element, suggesting that cis-regulatory structural variation underlies these mimetic adaptations. Our work shows that cortex functionally controls scale colour fate and that its cis-regulatory regions control a phenotypic switch in a modular and pattern-specific fashion
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Effects of temperature on the development of<i>Heliconius erato</i>butterflies
Anthropogenic climate change is thought to present a significant threat to biodiversity, in particular to tropical ectotherms, and the effects of long-term developmental heat stress on this group have received relatively little research attention. Here we study the effects of experimentally raising developmental temperatures in a tropical butterfly. We measured survival, development time, adult body mass, and wing size of a neotropical butterfly, Heliconius erato demophoon , across three temperature treatments. Egg survival was lower in the hotter treatments, with 83%, 73%, and 49% of eggs eclosing in the 20-30°C, 23-33°C, and 26-36°C treatments, respectively. Larval survival was five times lower in the 26-36°C treatment (4%) compared to the 20-30°C treatment (22%), and we did not detect differences in pupal survival across treatments due to high mortality in earlier stages. Adults in the 20-30°C treatment had a lower body mass and larvae had a lower growth rate compared to the intermediate 23-33°C treatment, but were heavier than the few surviving adults in the 26-36°C treatment. Females were heavier and grew faster as larvae than males in the 23-33°C treatment, but there was no associated increase in wing size. In summary, high developmental temperatures are particularly lethal for eggs and less so for larvae, and also affect adult morphology. This highlights the importance of understanding the effects of temperature variation across ontogeny in tropical ectotherms
Impacts of selective logging management on butterflies in the Amazon
Selective logging for timber production affects vast areas across the tropics, yet we lack detailed understanding of the impacts of logging intensity on biodiversity. These impacts can be studied at two levels: the impacts of logging intensity on overall diversity and community composition; and how logging intensity affects individual species' abundance-logging yield relationships. The latter underpins whether land-sharing logging (i.e. low intensity throughout) or land-sparing logging (i.e. high intensity with retention of some primary forest) is the optimal strategy. We examine both levels to determine the impacts of local-scale logging intensity on butterflies in Rondônia, Brazil, the global epicenter of butterfly alpha-diversity. Overall butterfly abundance was highest at intermediate logging intensity, whereas species richness increased after logging but was not affected by logging intensity, and that species composition increasingly changed from the primary community composition at higher logging intensities. Using individual species' abundance-yield curves, we then simulated species responses to a suite of logging strategies, ranging from total sharing to total sparing. Logging simulations predicted that more butterfly species would benefit from low-intensity land-sharing logging, having higher abundances than under land-sharing scenarios. However, some butterfly clades benefited disproportionally from the retention of primary forest within land-sparing logging concessions. Butterflies overall may benefit from intermediate logging strategies that promote a combination of low and high intensity logged areas, with some protected primary forest