Biology subjects

Jiggins, C. D.

Publications and source records attributed to Jiggins, C. D..

8 recordsLinked to original sources

bioRxiv2018

Genome-wide admixture is common across the Heliconius radiation

How frequent is gene flow between species? The pattern of evolution is typically portrayed as a phylogenetic tree, implying that speciation is a series of splits between lineages. Yet gene flow between good species is increasingly recognized as an important mechanism in the diversification of radiations, often spreading adaptive traits and leading to a complex pattern of phylogenetic incongruence. This process has thus far been studied in cases involving few species, or geographically restricted to spaces like islands, but not on the scale of a continental radiation. Previous studies have documented gene flow, adaptive introgression and hybrid speciation in a small subsection of the charismatic Neotropical butterflies Heliconius. Using genome-wide resequencing of 40 out of 45 species in the genus we demonstrate for the first time that admixture has played a role throughout the evolution of Heliconius and the sister genus Eueides. Modelling of phylogenetic networks based on 6848 orthologous autosomal genes (Maximum Pseudo-Likelihood Networks) or 5,483,419 high quality SNPs (Ancestral Recombination Graph) uncovers nine new cases of interspecific gene flow at up to half of the genome. However, f4 statistics of admixture show that the extent of the process has varied between subgenera. Evidence for introgression is found at all five loci controlling the colour and shape of the mimetic wing patterns, including in the putative hybrid species H. hecalesia, characterised by an unusual hindwing. Due to hybridization and incomplete coalescence during rapid speciation, individual gene trees show rampant discordance. Although reduced gene flow and faster coalescence are expected at the Z chromosome, we discover high levels of conflict between the 416 sex-linked loci. Despite this discordant pattern, both concatenation and multispecies coalescent approaches yield surprisingly consistent and fully supported genome-wide phylogenies. We conclude that the imposition of the bifurcating tree model without testing for interspecific gene flow may distort our perception of adaptive radiations and thus the ability to study trait evolution in a comparative framework.

evolutionary biology↗

bioRxiv2018

Generalisation behaviour of predators toward warning signals displayed by harmful prey: answers from a video-game played by humans.

The persistence of several warning signals in sympatry is a puzzling evolutionary question because selection favours convergence of colour patterns among toxic species. Such convergence is shaped by predators reaction to similar but not identical stimulus, i.e. generalisation behaviour. However, studying generalisation behaviour in complex natural communities of predators is challenging, and is thus generally limited to simple variations of prey colour patterns. Here, we used humans as surrogate predators to investigate generalisation behaviours on two prey communities with different level of warning signals complexity. Humans generalisation capacities were estimated using a computer game simulating a simple (4 morphs) and a complex (10 morphs) community of defended (associated with a penalty) and palatable butterflies. Colour patterns used in the game are actually observed in natural populations of the defended butterflies H. numata, and generalisation behaviour of natural predators communities on these colour patterns have previously been investigated in the wild, allowing direct comparison with human behaviour. We investigated human predation behaviour by recording attack rates on the different defended and palatable colour patterns, as well as player survival time (i.e. score). Phenotypic similarity among the different colour patterns was precisely quantified using a custom algorithm accounting for both colour and pattern variations (CPM method). By analysing attack behaviours of 491 game players, we found that learning was more efficient in the simple prey community. Additionally, profitable prey gained protection from sharing key visual features with unprofitable prey in both communities while learning, in accordance with natural predator behaviours. Moreover, other behaviours observed in natural predators, such as colour neophobia, were detected in humans and shaped morph vulnerability during the game. Similarities between our results in humans and the reaction of natural predator communities to the same colour patterns validate our video-game as a useful proxy to study predator behaviour. This experimental set-up can thus be compared to natural systems, enabling further investigations of generalisation on mimicry evolution.

evolutionary biology↗

bioRxiv2018

Sexually dimorphic gene expression and transcriptome evolution provides mixed evidence for a fast-Z effect in Heliconius

Sex chromosomes have different evolutionary properties as compared to the autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution in the sex chromosomes of a group of tropical butterflies. We first improved the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then we sequenced RNA from male and female whole abdomens and female ovary and gut tissue to identify sex and tissue specific gene expression profiles in H. melpomene. Using these expression profiles we compare sequence divergence and polymorphism, the strength of positive and negative selection and rates of adaptive evolution for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato.\n\nWe show that the rate of adaptive substitutions is higher for Z as compared to autosomal genes, but contrary to expectation it is also higher for male as compared to female biased genes. There is therefore mixed evidence that hemizygosity influences the rate of adaptive substitutions. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic specific tissue. Together our results provide limited support for fast-Z evolution. This contributes to a growing body of literature from other ZW systems that also provide mixed evidence for a fast-Z effect.

evolutionary biology↗

bioRxiv2018

Male pheromone composition depends on larval but not adult diet in Heliconius melpomene

Condition-dependent traits can act as honest signals of mate quality, with fitter individuals able to display preferred phenotypes. Nutrition is known to be an important determinant of individual condition, with diet known to affect many secondary sexual traits. In Heliconius butterflies, male chemical signalling plays an important role in female mate choice. Heliconius pheromones are sexually dimorphic, found only in mature males, but it is unclear what information they convey to the female. Here, we manipulate both the larval and adult diet of male Heliconius melpomene rosina to test for environmental effects on wing and genital pheromone production. We find no evidence that adult pollen consumption affects pheromone production in the first ten days after eclosion. We also find strong overlap in the chemical profiles of individuals reared on different larval host plants. However, individual compounds were found in different amounts between host plant treatments. Further electrophysiological and behavioural experiments will be needed to determine the biological significance of these differences.

ecology↗

bioRxiv2017

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a large-X effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on the sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, i.e. faster-X, or barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply post-zygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of species incompatibilities. Our work demonstrates the importance of constructing an appropriate demographic null model in order to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.

evolutionary biology↗

bioRxiv2017

What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies.

The process by which species evolve can be illuminated by investigating barriers that limit gene flow between taxa. Recent radiations, such as Heliconius butterflies, offer the opportunity to compare isolation between pairs of taxa at different stages of ecological, geographic and phylogenetic divergence. We carry out a comparative analysis of existing and novel data in order to quantify the strength and direction of isolating barriers within a well-studied clade of Heliconius. Our results highlight that increased divergence is associated with the accumulation of stronger and more numerous barriers to gene flow. Wing pattern is both under natural selection for Mullerian mimicry and involved in mate choice, and therefore underlies several isolating barriers. However, pairs which share a similar wing pattern, also display strong reproductive isolation mediated by traits other than wing pattern. This suggests that, while wing pattern is a key factor for early stages of divergence, it is not essential at a higher level. Additional factors including habitat isolation, hybrid sterility and chemically-mediated mate choice are associated with complete speciation. Therefore, although most previous work has emphasised the role of wing pattern, our comparative results highlight that speciation is a multidimensional process, whose completion is stabilized by many factors.

evolutionary biology↗

bioRxiv2017

North Andean origin and diversification of the largest ithomiine butterfly genus

The Neotropics harbour the most diverse flora and fauna on Earth. The Andes are a major centre of diversification and source of diversity for adjacent areas in plants and vertebrates, but studies on insects remain scarce, even though they constitute the largest fraction of terrestrial biodiversity. Here, we combine molecular and morphological characters to generate a dated phylogeny of the butterfly genus Pteronymia (Nymphalidae: Danainae), which we use to infer spatial, elevational and temporal diversification patterns. We first propose six taxonomic changes that raise the generic species total to 53, making Pteronymia the most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows that Pteronymia originated in the Northern Andes, where it diversified extensively. Some lineages colonized lowlands and adjacent montane areas, but diversification here remained scarce. The recent colonization of lowland areas was reflected by an increase in the rate of evolution of species elevational ranges towards present. By contrast, speciation rate decelerated with time, with no extinction. The geological history of the Andes and adjacent regions have likely contributed to Pteronymia diversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others.

evolutionary biology↗

bioRxiv2016

Recombination Suppression is Unlikely to Contribute to Speciation in Sympatric Heliconius Butterflies

Mechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of co-adapted gene combinations. The sympatric butterfly species H. melpomene and H. cydno are separated by many strong barriers, but the species still hybridise infrequently in the wild, with around 40% of the genome influenced by introgression. We tested the hypothesis that genetic barriers between the species are reinforced by inversions or other mechanisms to reduce between-species recombination rate. We constructed fine-scale recombination maps for Panamanian populations of both species and hybrids to directly measure recombination rate between these species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno.\n\nAuthor SummaryIt is now possible to study the process of species formation by sequencing the genomes of multiple closely related species. Heliconius melpomene and Heliconius cydno are two butterfly species that have diverged over the past 2 million years and have different colour patterns, mate preferences and host plants. However, they still hybridise infrequently in the wild and exchange large parts of their genomes. Typically, when genomes are exchanged, chromosomes are recombined and gene combinations are broken up, preventing species from forming. Theory predicts that gene variants that define species might be linked together because of structural differences in their genomes, such as inverted pieces of chromosomes that will not be broken up when the species hybridise. However, in this paper, we use deep sequencing of large crosses of butterflies to show that there are no long chromosome regions that are not broken up during hybridisation, and no long chromosome inversions anywhere between the two genomes. This suggests that hybridisation is rare enough and mate preference is strong enough that inversions are not necessary to maintain the species barrier.

evolutionary biology↗