Showing papers by "Camilo Salazar published in 2020"

Selective sweeps on novel and introgressed variation shape mimicry loci in a butterfly adaptive radiation.

Abstract: Natural selection leaves distinct signatures in the genome that can reveal the targets and history of adaptive evolution. By analysing high-coverage genome sequence data from 4 major colour pattern loci sampled from nearly 600 individuals in 53 populations, we show pervasive selection on wing patterns in the Heliconius adaptive radiation. The strongest signatures correspond to loci with the greatest phenotypic effects, consistent with visual selection by predators, and are found in colour patterns with geographically restricted distributions. These recent sweeps are similar between co-mimics and indicate colour pattern turn-over events despite strong stabilising selection. Using simulations, we compare sweep signatures expected under classic hard sweeps with those resulting from adaptive introgression, an important aspect of mimicry evolution in Heliconius butterflies. Simulated recipient populations show a distinct 'volcano' pattern with peaks of increased genetic diversity around the selected target, characteristic of sweeps of introgressed variation and consistent with diversity patterns found in some populations. Our genomic data reveal a surprisingly dynamic history of colour pattern selection and co-evolution in this adaptive radiation.

Chemical signals act as the main reproductive barrier between sister and mimetic Heliconius butterflies.

Abstract: Colour pattern is the main trait that drives mate recognition between Heliconius species that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatri...

Species specificity and intraspecific variation in the chemical profiles of Heliconius butterflies across a large geographic range

Abstract: In many animals, mate choice is important for the maintenance of reproductive isolation between species. Traits important for mate choice and behavioral isolation are predicted to be under strong stabilizing selection within species; however, such traits can also exhibit variation at the population level driven by neutral and adaptive evolutionary processes. Here, we describe patterns of divergence among androconial and genital chemical profiles at inter- and intraspecific levels in mimetic Heliconius butterflies. Most variation in chemical bouquets was found between species, but there were also quantitative differences at the population level. We found a strong correlation between interspecific chemical and genetic divergence, but this correlation varied in intraspecific comparisons. We identified "indicator" compounds characteristic of particular species that included compounds already known to elicit a behavioral response, suggesting an approach for identification of candidate compounds for future behavioral studies in novel systems. Overall, the strong signal of species identity suggests a role for these compounds in species recognition, but with additional potentially neutral variation at the population level.

Deep Convergence, Shared Ancestry, and Evolutionary Novelty in the Genetic Architecture of Heliconius Mimicry.

Abstract: Convergent evolution can occur through different genetic mechanisms in different species. It is now clear that convergence at the genetic level is also widespread, and can be caused by either (i) parallel genetic evolution, where independently evolved convergent mutations arise in different populations or species, or (ii) collateral evolution in which shared ancestry results from either ancestral polymorphism or introgression among taxa. The adaptive radiation of Heliconius butterflies shows color pattern variation within species, as well as mimetic convergence between species. Using comparisons from across multiple hybrid zones, we use signals of shared ancestry to identify and refine multiple putative regulatory elements in Heliconius melpomene and its comimics, Heliconius elevatus and Heliconius besckei, around three known major color patterning genes: optix, WntA, and cortex While we find that convergence between H. melpomene and H. elevatus is caused by a complex history of collateral evolution via introgression in the Amazon, convergence between these species in the Guianas appears to have evolved independently. Thus, we find adaptive convergent genetic evolution to be a key driver of regulatory changes that lead to rapid phenotypic changes. Furthermore, we uncover evidence of parallel genetic evolution at some loci around optix and WntA in H. melpomene and its distant comimic Heliconius erato Ultimately, we show that all three of convergence, conservation, and novelty underlie the modular architecture of Heliconius color pattern mimicry.

An exploration of the complex biogeographical history of the Neotropical banner-wing damselflies (Odonata: Polythoridae)

Abstract: The New World Tropics has experienced a dynamic landscape across evolutionary history and harbors a high diversity of flora and fauna While there are some studies addressing diversification in Neotropical vertebrates and plants, there is still a lack of knowledge in arthropods Here we examine temporal and spatial diversification patterns in the damselfly family Polythoridae, which comprises seven genera with a total of 58 species distributed across much of Central and South America Our time-calibrated phylogeny for 48 species suggests that this family radiated during the late Eocene (~ 33 Ma), diversifying during the Miocene As with other neotropical groups, the Most Recent Common Ancestor (MRCA) of most of the Polythoridae genera has a primary origin in the Northern Andes though the MRCA of at least one genus may have appeared in the Amazon Basin Our molecular clock suggests correlations with some major geographical events, and our biogeographical modeling (with BioGeoBEARS and RASP) found a significant influence of the formation of the Pebas and Acre systems on the early diversification of these damselflies, though evidence for the influence of the rise of the different Andean ranges was mixed Diversification rates have been uniform in all genera except one—Polythore—where a significant increase in the late Pliocene (~ 3 mya) may have been influenced by recent Andean uplift The biogeographical models implemented here suggest that the Pebas and Acre Systems were significant geological events associated with the diversification of this damselfly family; while diversification in the tree shows some correlation with mountain building events, it is possible that other abiotic and biotic changes during our study period have influenced diversification as well The high diversification rate observed in Polythore could be explained by the late uplift of the Northern Andes However, it is possible that other intrinsic factors like sexual and natural selection acting on color patterns could be involved in the diversification of this genus

Müllerian mimicry of a quantitative trait despite contrasting levels of genomic divergence and selection

Abstract: Hybrid zones, where distinct populations meet and interbreed, give insight into how differences between populations are maintained despite gene flow. Studying clines in genetic loci and adaptive traits across hybrid zones is a powerful method for understanding how selection drives differentiation within a single species, but can also be used to compare parallel divergence in different species responding to a common selective pressure. Here, we study parallel divergence of wing colouration in the butterflies Heliconius erato and H. melpomene , which are distantly related Mullerian mimics which show parallel geographic variation in both discrete variation in pigmentation, and quantitative variation in structural colour. Using geographic cline analysis, we show that clines in these traits are positioned in roughly the same geographic region for both species, which is consistent with direct selection for mimicry. However, the width of the clines varies markedly between species. This difference is explained in part by variation in the strength of selection acting on colour traits within each species, but may also be influenced by differences in the dispersal rate and total strength of selection against hybrids between the species. Genotyping‐by‐sequencing also revealed weaker population structure in H. melpomene , suggesting the hybrid zones may have evolved differently in each species, which may also contribute to the patterns of phenotypic divergence in this system. Overall, we conclude that multiple factors are needed to explain patterns of clinal variation within and between these species, although mimicry has probably played a central role.

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

Abstract: Species divergence is facilitated when traits under divergent selection also act as mating cues. Fluctuations in sensory conditions can alter signal perception independently of adaptation to contrasting sensory environments, but how this fine scale variation affects behavioural isolation has received less attention, especially in terrestrial organisms. The warning patterns of Heliconius butterflies are under selection for aposematism and act as mating cues. Using computer vision, we extracted behavioural data from 1481 hours of video footage for 387 individuals. We show that the putative hybrid species H. heurippa and its close relative H. timareta linaresi differ in their response to divergent warning patterns, and that these differences are strengthened with increased local illuminance. Trials with live individuals reveal low-level assortative mating that are sufficiently explained by differences in visual attraction. Finally, results from hybrid butterflies are consistent with linkage between a major warning pattern gene and the corresponding behaviour, though the differences in behaviour we observe are unlikely to cause rapid reproductive isolation as predicted under a model of hybrid trait speciation. Overall, our results highlight that the role of ecological mating cues for behavioural isolation may depend on the immediate sensory conditions during which they are displayed to conspecifics.

Mullerian mimicry of a quantitative trait despite contrasting levels of genomic divergence and selection

Abstract: Hybrid zones, where distinct populations meet and interbreed, give insight into how differences between populations are maintained despite gene flow. Studying clines in genetic loci and adaptive traits across hybrid zones is a powerful method for understanding how selection drives differentiation within a single species, but can also be used to compare parallel divergence in different species responding to a common selective pressure. Here, we study parallel divergence of wing colouration in the butterflies Heliconius erato and H. melpomene, which are distantly related Mullerian mimics that show parallel geographic variation in both discrete variation in pigmentation, and quantitative variation in structural colour. Using geographic cline analysis, we show that clines in these traits are positioned in the roughly the same geographic region for both species, which is consistent with direct selection for mimicry. However, the width of the clines varies markedly between species. This difference is explained in part by variation in the strength of selection acting on colour traits within each species, but may also be influenced by differences in the dispersal rate and total strength of selection against hybrids between the species. Genotyping-by-sequencing also revealed weaker population structure in H. melpomene, suggesting the hybrid zones may have evolved differently in each species; which may also contribute to the patterns of phenotypic divergence in this system Overall, we conclude that multiple factors are needed to explain patterns of clinal variation within and between these species, although mimicry has probably played a central role.