Biology subjects

Pardo-Diaz, C.

Publications and source records attributed to Pardo-Diaz, C..

15 recordsLinked to original sources

bioRxiv2026

Adaptation in the eye and brain contributes to species divergence in visual perception in Heliconius butterflies

Sensory systems mediate the interaction between organisms and their environment, but how complex sensory pathways evolve and relate to variation in perception and behavior across ecological contexts, remains poorly understood, especially for terrestrial taxa. Here, we investigate whole-visual-system adaptation in Heliconius erato butterflies. Using continent-wide sampling, we demonstrate that within H. erato, facet count significantly decreased with increasing elevation. Common-garden rearing of low-elevation H. erato populations from Ecuador and their high-elevation sister species, H. himera, showed that eye and brain morphology are heritable, and comparisons to genomic measures of divergence indicates that this variation is due to divergent selection. Parallel comparisons from Colombia involving H. chestertonii (high elevation) and H. erato venus (low elevation) further revealed that eye and brain morphology can evolve as independent, decoupled traits. For both locations, differences in visual acuity correlated with variation in facet count. We also observed parallel evolution of spectral sensitivity, with independent high-elevation populations having fewer red-reflecting lateral filtering pigments. To experimentally link visual system morphology to behavior, we assessed visual acuity in second-generation H. erato cyrbia-H. himera hybrids. Overall, acuity was influenced by facet count, and when analyzed together with brain morphology, by a positive interaction between facet count and optic lobe volume, demonstrating that structural investment in the eye and neural expansion combine to maximize visual perception. This work shows that visual adaptation is a multi-layered process whereby sensory traits can evolve independently under localized ecological pressures, but evolution across the visual pathway contributes to refinements in behavioral performance.

evolutionary biology↗

bioRxiv2026

Rapid speciation in Harlequin Toads (Anura: Bufonidae) endemic to the Sierra Nevada de Santa Marta

The Neotropical genus Atelopus has experienced a drastic population decline in recent decades. Despite this, a knowledge gap remains regarding the conservation genetic status, phylogeography, and demographic history of most of its species, especially those endemic to areas with limited access like the Sierra Nevada de Santa Marta in Colombia. In this genomic study, we inferred phylogenetic relationships, demographic history, and gene flow among four endemic Atelopus morphospecies in the Sierra Nevada de Santa Marta-SNSM. Additionally, we compared the effective population size (Ne) estimates with the available population census data. NextRAD was used to obtain genomic data from 95 individuals collected at five sites in the SNSM and two in the Colombian Pacific (outgroup). The morphospecies recently diverged in a scenario without gene flow and were recovered as monophyletic. Their phylogenetic relationships were discordant, which is attributed to the presence of incomplete lineage sorting-ILS, which would also explain their shared ancestry among them. The lack of gene flow as well as the recent divergence times given by demography suggests a recent and rapid speciation. However, the reproductive isolation mechanisms that promote or maintain the species boundaries in this group remain unknown and require further investigation. We suggest that this process may have been influenced by the complex topography of the SNSM, traits such as high philopatry, low dispersal ability, and behavioral factors such as habitat preference or to factors related to genetic architecture that influenced the rapid formation of reproductive barriers among populations. Additionally, a pattern of population decline was observed around 200.000 years ago, with recent increases in three morphospecies. Despite the reduction in effective population size, no signs of inbreeding were detected. However, for A. laetissimus, the only species surveyed, the estimated value of Ne and its implications should be interpreted with caution. Ultimately, our findings reveal an evolutionary history shaped by a burst of diversification and abrupt reproductive isolation, highlighting how the resulting endemism and restricted genetic connectivity shape the unique evolutionary trajectory and vulnerability of this threatened montane species. Significance StatementThe mechanisms driving rapid speciation in montane ecosystems remain a central question in evolutionary biology. This study provides crucial genomic insights into the diversification of four endemic Atelopus species in an isolated Neotropical massif. We reveal a compelling evolutionary scenario where species diverge rapidly in absence of gene flow. This rapid speciation was likely facilitated by complex topography, environmental heterogeneity, and ecological and behavioral differences among species. Nevertheless, the evolutionary processes that limited gene flow among SNSM species have not yet been identified.

evolutionary biology↗

bioRxiv2026

Ecological divergence and post-eclosion brain development shape visual performance during Heliconius speciation

Sensory adaptation is increasingly recognized as a key driver of ecological speciation, but how visual system divergence is coordinated across development, and how this translates into behavioral differences, remains poorly understood. The butterfly Heliconius cydno, which inhabits closed-canopy forests, has larger eyes and greater investment in visual brain centers than its sympatric close-relative H. melpomene, which occupies more open forest-edge habitats, suggesting divergent ecological selection on the visual system. However, the behavioral consequences of these visual adaptations, their developmental trajectories, and whether they break down in hybrids is unknown. To address these questions, we combined ecological field data with behavioral assays and deep-learning-assisted segmentation of neuroanatomy. Visual acuity - the ability to resolve spatial detail - was higher in H. cydno, consistent with its greater ommatidia number, but also increased with age in both species despite no change in external eye morphology. These improvements coincided with the onset of male courtship and female oviposition, suggesting that early adult neurodevelopment shapes visual performance and may support the demands of reproduction. Brain morphology showed species-specific trajectories of post-eclosion optic lobe growth that broadly paralleled increases in acuity and were accompanied by ongoing neurogenesis in the adult optic lobes. While hybrids exhibited intermediate visual acuity, relationships among different components of the visual system were disrupted in hybrids. Together, these results show that ommatidia number alone cannot explain variation in visual acuity, and highlight how coordinated sensory evolution, and its breakdown in hybrids, may contribute to divergence during the early stages of speciation. Significance StatementAdaptation of sensory systems is increasingly recognized as a key driver of species formation, but it is unclear how these systems develop and shape behavioral differences. Using closely related Heliconius butterflies adapted to different light environments, we show that visual acuity improves during early adulthood through neural development, despite no change in eye structure. This maturation coincides with the onset of reproductive behaviors and is accompanied by growth and neurogenesis in visual brain regions. In hybrids, coordination among sensory traits breaks down, resulting in intermediate visual performance. These results show that sensory development is critical for behavioral adaptation and suggest that its integration contributes to the maintenance of species boundaries.

evolutionary biology↗

bioRxiv2024

Repeated evolution of reduced visual investment at the onset of ecological speciation in high-altitude Heliconius butterflies.

Colonisation of new habitats is typically followed by divergent selection acting on traits that are immediately important for fitness in the new habitat. For example, shifting sensory environments are often associated with variation in sensory traits critical for navigation and foraging. However, the extent to which the initial response to novel sensory conditions is mediated by phenotypic plasticity, and its contribution to early species divergence remains unclear. We took advantage of repeated cases of speciation in Heliconius butterflies with independent allopatric distributions in the west of the Colombian and Ecuadorian Andes. Using volumetric brain measurements, we analysed patterns of investment in sensory processing in brain components across different localities and habitats. We find that a higher-altitude species, H. chestertonii, differs in levels of investment in visual and olfactory brain centres compared to its lower altitude relative H. erato venus, mainly attributable to heritable variation as inferred from comparisons between wild and common-garden reared individuals. We compared these shifts with those reported for another high-altitude species, H. himera, and its parapatric lowland counterpart, H. erato cyrbia, and demonstrate parallel reductions in the size of specific optic lobe neuropils. Conversely, for the antennal lobe, we detected disparate trait shifts in H. himera and H. chestertonii in respect to their lowland erato neighbours. Overall, our findings add weight to the adaptive potential for neuroanatomical divergence related to sensory processing during early species formation. Lay summaryRepeated associations between trait variation and environmental shifts may indicate adaptation to local sources of natural selection. For instance, in fish, the presence of certain morphological traits in specific ecological conditions across independent populations is well documented, suggesting equivalent phenotypic responses to shared sources of natural selection. We compared independent cases of ecological divergence in Heliconius butterflies distributed along altitude gradients from sea level to mid mountain in the west of the Colombian and Ecuadorian Andes. Shifts in altitude involve repeated, abrupt transitions from wet, large-leaved, warm forests to higher dry, open, cold scrubs. We tested hypotheses about the role of these ecological shifts in driving adaptive evolution in neuroanatomical traits during early speciation. We showed that in Heliconius, independent changes in forest-type have been accompanied by heritable parallel patterns of divergence in sensory investment in visual processing in the brain. We propose these differences likely facilitate species divergence in the face of ongoing geneflow.

evolutionary biology↗

bioRxiv2024

Sensory weighting reflects changing patterns of visual investment during ecological divergence in Heliconius butterflies.

Integrating information across sensory modalities enables animals to orchestrate a wide range of complex behaviours. The relative importance placed on one sensory modality over another reflects the reliability of cues in a particular environment and corresponding differences in neural investment. As populations diverge across environmental gradients, the reliability of sensory cues may shift, favouring divergence in neural investment and the weight given to different sensory modalities. During their divergence across closed-forest and forest-edge habitats, closely related butterflies Heliconius cydno and H. melpomene evolved distinct brain morphologies, with the former investing more in vision. Quantitative genetic analyses suggest selection drove these changes, but their behavioural effects remain uncertain. We hypothesised that divergent neural investment may alter sensory weighting. We trained individuals in an associative learning experiment using multimodal colour and odour cues. When positively rewarded stimuli were presented in conflict pairing positively trained colour with negatively trained odour, and vice-versa, H. cydno favoured visual cues more strongly than H. melpomene. Hence, differences in sensory weighting may evolve early during divergence and are predicted by patterns of neural investment. These findings, alongside other examples, imply that differences in sensory weighting stem from divergent investment as adaptations to local sensory environments.

evolutionary biology↗

bioRxiv2023

Divergent warning patterns influence male and female mating behaviours in a tropical butterfly

Traits under divergent ecological selection that also function during mating can be important in maintaining species boundaries. Few studies have considered mutual mate choice, where both males and females base mating decisions on the same trait. We investigated the contribution of visual preference to assortative mating between an aposematic butterfly Heliconius cydno and its sympatric relative H. melpomene. Wing colouration in Heliconius butterflies evolved as a warning signal but also functions as a mating cue. We predicted that both sexes of H. cydno contributed to assortative mating by exhibiting visual preference towards conspecific wing colouration. We analysed published and new data from preference experiments, in which males were presented with conspecific and H. melpomene females. We also recorded female responses and mating outcomes in choice experiments, involving conspecific males with either the original white or artificially painted red forewing bands. Both sexes of H. cydno responded more positively towards the conspecific colouration, yet male colouration did not predict mating outcomes in female choice experiments. As courtships are initiated by males in butterflies, our findings suggest that female visual preference might be of secondary importance in preventing gene flow between H. cydno and H. melpomene.

animal behavior and cognition↗

bioRxiv2023

Adaptive introgression of a visual preference gene

Visual preferences are important drivers of mate choice and sexual selection, but little is known of how they evolve at the genetic level. Here we take advantage of the diversity of bright warning patterns displayed by Heliconius butterflies, which are also used during mate choice. We show that two Heliconius species have evolved the same visual mating preferences for females with red patterns by exchanging genetic material through hybridization. Extensive behavioral experiments reveal that male preferences are associated with a genomic region of increased admixture between these two species. Variation in neural expression of regucalcin1, located within this introgressed region, correlates with visual preference across populations, and disruption of regucalcin1 with CRISPR/Cas9 impairs courtship towards conspecific females, proving a direct link between gene and behavior. Our results support a role for hybridization during behavioral evolution, and show how visually-guided behaviors contributing to adaptation and speciation are encoded within the genome.

evolutionary biology↗

bioRxiv2023

Parallel shifts in flight-height associated with altitude across incipient Heliconius species

Vertical gradients in microclimate, resource availability and interspecific interactions are thought to underly stratification patterns in tropical insect communities. However, only a few studies have explored the adaptive significance of vertical space use during early population divergence. We analysed flight-height variation across speciation events in Heliconius butterflies representing parallel instances of divergence between low and high-altitude populations. We measured flight-height in wild H. erato venus and H. chestertonii, lowland and mountain specialists respectively, and found that H. chestertonii consistently flies at a lower height. We compared these data with previously published results for H. e. cyrbia and H. himera, the latter of which flies lower and, like H. chestertonii, recently colonised high-altitude, dry forests. We show that these repeated trends largely result from shared patterns of selection across equivalent environments, producing parallel trait-shifts in H. himera and H. chestertonii. Although our results imply a signature of local adaptation, we did not find an association between resource distribution and flight-height in H. e. venus and H. chestertonii. We discuss how this pattern may be explained by variation in forest structure and microclimate. Overall, our findings underscore the importance of behavioural adjustments during early divergence mediated by altitude-shifts.

evolutionary biology↗

bioRxiv2023

Sex chromosome - autosome fusions in Heliconius butterflies

Sex chromosomes are evolutionarily labile in many animals and sometimes fuse with autosomes, creating so-called neo-sex chromosomes. Fusions between sex chromosomes and autosomes have been proposed to reduce sexual conflict and to promote adaptation and reproductive isolation among species. Recently, advances in genomics have fuelled the discovery of such fusions across the tree of life. Here, we discovered multiple fusions leading to neo-sex chromosomes in the sara/sapho clade of the classical adaptive radiation of Heliconius butterflies. Heliconius butterflies generally have 21 chromosomes with very high synteny. However, the five species in the sapho subclade show large variation in chromosome number ranging from 21 to 60. We found that the W chromosome is fused with chromosome 4 in all of them. Two sister species pairs showed subsequent fusions between the W and chromosomes 9 or 14, respectively. These sequential fusions between autosomes and sex chromosomes make Heliconius butterflies an ideal system for studying the role of neo-sex chromosomes in adaptive radiations and the degeneration of sex chromosomes over time. Our findings emphasize the capability of WGS technology to detect neo-sex chromosomes even when sex chromosomes are not explicitly assembled. Author SummaryFusions between sex chromosomes and autosomes are thought to have the potential to resolve sexual conflict and enhance local adaptation or reproductive isolation between species. Here, we discovered such fusions in Heliconius butterflies. Heliconius butterflies mostly have a very stable karyotype with 21 chromosomes and high synteny across species. However, the five species in the sapho subclade have up to 60 chromosomes, suggesting that they have undergone many chromosomal fissions. We document that in addition to the fissions, the sapho subclade also showed multiple fusions between the female-specific sex chromosome (W) and autosomes. We found a W-4 fusion shared by all five species and additional W fusions with chromosomes 9 and 14 shared by two species each. Even though in many sapho subclade species the autosomes have undergone fissions, the chromosomes fused with the W represent the full-length autosomes, as seen in other Heliconius species, suggesting that fusing to the W protected them from fissions. Our study reveals the power of short-read sequencing to discover neo-sex chromosomes and showcases Heliconius butterflies as a promising system for studying the causes and consequences of sex chromosome evolution.

evolutionary biology↗

bioRxiv2022

Does sexual conflict contribute to the evolution of novel warning patterns?

Why warning patterns are so diverse is an enduring evolutionary puzzle. Because predators associate particular patterns with unpleasant experiences, an individuals predation risk should decrease as the local density of its warning pattern increases, promoting pattern monomorphism. Distasteful Heliconius butterflies are known for their diversity of warning patterns. Here, we explore whether interlocus sexual conflict can contribute to their diversification. Male Heliconius use warning patterns as mating cues, but mated females may suffer costs if this leads to harassment, favoring novel patterns. Using simulations, we show that drift alone is unlikely to cause pattern diversification, but that sexual conflict can assist such process. We also find that genetic architecture influences the evolution of male preferences, which track changes in warning pattern due to sexual selection. When male attraction imposes costs on females, this affects the speed at which novel pattern alleles increase. In two experiments, females laid fewer eggs with males present. However, although males in one experiment showed less interest in females with manipulated patterns, we found no evidence that female coloration mitigates sex-specific costs. Overall, male attraction to conspecific warning patterns may impose an unrecognized cost on Heliconius females, but further work is required to determine this experimentally.

evolutionary biology↗

bioRxiv2020

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

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.

evolutionary biology↗

bioRxiv2020

Phylogenetic signal is associated with the degree of variation in root-to-tip distances

The phylogenetic information contained in sequence data is partly determined by the overall rate of nucleotide substitution in the genomic region in question. However, phylogenetic signal is affected by various other factors, such as heterogeneity in substitution rates across lineages. These factors might be able to predict the phylogenetic accuracy of any given gene in a data set. We examined the association between the accuracy of phylogenetic inference across genes and several characteristics of branch lengths in phylogenomic data. In a large number of published data sets, we found that the accuracy of phylogenetic inference from genes was consistently associated with their mean statistical branch support and variation in their gene tree root-to-tip distances, but not with tree length and stemminess. Therefore, a signal of constant evolutionary rates across lineages appears to be beneficial for phylogenetic inference. Identifying the causes of variation in root-to-tip lengths in gene trees also offers a potential way forward to increase congruence in the signal across genes and improve estimates of species trees from phylogenomic data sets.

evolutionary biology↗

bioRxiv2020

Urban colonization is driven by a mixture of evolutionarily conserved and labile traits

Urbanization is a fast and dramatic transformation of habitat that generally forces native fauna into novel ecological challenges. The biological prerequisites necessary to establish in urban areas have been widely studied, but the macroevolutionary characteristics of traits that allow urban colonization remain poorly understood. Urban colonization might be facilitated by traits that are evolutionarily conserved and which lead to a diversity of closely related species. Alternatively, urban colonization might be associated with labile traits that frequently arise and are lost. In a large data set from passerine birds, we find that urban colonization has a signal of highly labile traits, despite many traits associated with colonization being highly conserved. Urban colonization is associated with traits that allow faster speciation than non-urban-colonizing counterparts, and more frequently transition to non-urban trait states than in the opposite direction. Overall, the traits that facilitate urban colonization are a mix of highly conserved and labile traits and appear to provide an evolutionarily successful strategy.

evolutionary biology↗

bioRxiv2019

Parallel clines in a quantitative trait in butterfly co-mimics species despite different levels of genomic divergence and selection

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.

evolutionary biology↗

bioRxiv2018

Gene flow and Andean uplift shape the diversification of Gasteracantha cancriformis (Araneae: Araneidae) in Northern South America

AimThe Andean uplift has played a major role shaping the current Neotropical biodiversity. However, in arthropods other than butterflies, little is known about how this geographic barrier has impacted species historical diversification. Here we examined the phylogeography of the widespread and color polymorphic spider Gasteracantha cancriformis to: (i) evaluate the effect of the northern Andean uplift on its divergence and, (ii) assess whether its diversification occurred in the presence of gene flow.\n\nLocationNorthern Andes and Brazil\n\nMethodsWe inferred phylogenetic relationships and divergence times in G. cancriformis using mitochondrial and nuclear data from 105 individuals in northern South America. Genetic diversity, divergence and population structure were quantified. We also compared multiple demographic scenarios for this species using a model-based approach (PHRAPL) to establish divergence with or without gene flow. Finally, we evaluated the association between genetic variation and color polymorphism.\n\nResultsBoth nuclear and mitochondrial data supported two well-differentiated clades, which correspond to populations occurring in opposite sides of the Eastern cordillera of the Colombian Andes. The splitting between these clades occurred in the early Pleistocene, around 2.13 million years ago (95% HPD = 0.98-3.93).\n\nDespite this vicariant event, there is shared genetic variation between the clades, which is better explained by a scenario of historical divergence in the face of gene flow. Color polymorphism was randomly scattered in both clades and is not statistically associated with the genetic variation studied here.\n\nMain ConclusionsThe final uplift of Eastern cordillera of the Colombian Andes was identified as the major force that shaped the diversification of G. cancriformis in Northern South America, resulting in a cis- and trans-Andean phylogeographic structure for the species. The divergence in the face of gene flow between cis- and trans-Andean populations found for this spider has been likely facilitated by the presence of low-elevation passes across the Eastern Colombian cordillera. Our work constitutes the first example where the Andean uplift coupled with gene flow influenced the evolutionary history of an arachnid lineage.

evolutionary biology↗