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McMillan, O.

Publications and source records attributed to McMillan, O..

4 recordsLinked to original sources

Replaying the Tape: Comparative Genomics of Color Pattern in Heliconius

Understanding the repeatability of evolution requires disentangling the roles of constraint, contingency, and convergence in shaping phenotypic diversity. Mullerian mimicry in Heliconius butterflies offers a powerful natural experiment, with co-occurring species independently evolving similar wing color patterns under shared selective regimes. Here, we integrate high-throughput image-based phenotyping, genome-wide association studies (GWAS), and comparative pan-genomics to investigate the genetic architecture underlying convergent wing pattern evolution across parallel hybrid zones in Heliconius erato and H. melpomene. Using automated computer vision pipelines, we extracted and quantified color pattern variation from over 650 butterfly specimens. Principal component analysis (PCA) of recolorized, landmark-aligned wing images captured biologically meaningful axes of variation, which were used as phenotypes in GWAS. We identified strong associations at known patterning loci--including ivory:mir193 (previously coretex), optix, WntA, and vvl--as well as novel regions, including a chromosome 2 inversion in H. erato and a gustatory receptor gene (Gr21a) in H. melpomene. Comparative analyses using a Heliconius pan-genome revealed that while significant associations mapped to homologous regulatory regions across species, the specific variants were lineage-specific, consistent with parallel evolution via distinct cis-regulatory changes. These findings demonstrate that repeated adaptive outcomes can arise through different genetic paths within conserved regulatory architectures. More broadly, our study highlights the power of integrating machine learning, high-resolution phenotyping, and comparative genomics to dissect the molecular basis of convergent evolution in natural populations.

evolutionary biology↗

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↗

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

Colour pattern has been long recognised as the trait that drives mate recognition between Heliconius species that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatric and closely related species, alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related species Heliconius melpomene malleti and H. timareta florencia, occur in the same geographic region and despite being co-mimics they display strong reproductive isolation. In order to test which cues differ between species, and therefore potentially contribute to reproductive isolation, we quantified differences in wing phenotype and male chemical profile. As expected, wing colour pattern was indistinguishable between the two species while the chemical profile of their male sex pheromones showed marked differences. We then conducted behavioural experiments to study the importance of these signals in mate recognition by females. In agreement with our previous results, we found that pheromones and not wing colour pattern drive the preference of females by conspecific males. In addition, experiments with hybrid males and females suggested an important genetic component for both pheromone production and preference. Altogether, these results suggest that pheromones are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.

evolutionary biology↗

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↗