Biology subjects

Briscoe, A. D.

Publications and source records attributed to Briscoe, A. D..

8 recordsLinked to original sources

bioRxiv2025

Phylogeny, systematics and evolution of mimicry patterns in Neotropical limenitidine butterflies

The Neotropical butterfly genus Adelpha Hubner exhibits remarkable species diversity and striking convergence in wing colour patterns potentially explained by mimicry, making it an exceptional model for exploring trait evolution and its relationship with speciation. To date, unresolved phylogenetic relationships hinder a comprehensive understanding of the evolutionary biology of the genus. Using a novel multi-marker dataset combining one mitochondrial and 15 nuclear gene fragments, we generate the most comprehensive phylogeny of the genus Adelpha to revisit its systematics and investigate the evolution of mimicry colour patterns. Our data set encompasses 83 of the 87 known extant species and six Limenitis species that were recently excluded from Adelpha (134 of c. 160 subspecies in total), collectively displaying 14 distinct mimicry patterns. We provide conclusive evidence that corroborates previous work on the polyphyly of Adelpha as historically conceived, and describe the genus Adelphina Paez & Willmott n. gen. to stabilize the nomenclature, both genera representing Neotropical limenitidines. The comprehensive phylogeny provided in this study lays a solid foundation for future research into the processes driving diversification within these species interacting through mimicry. Ancestral character state reconstruction reveals gradual evolution of mimicry pattern. The more common mimicry pattern IPHICLUS (forewing with orange subapical spot and white band) is inferred as ancestral, but repeated convergent evolution is also recovered. Evolutionary convergence is also observed for the second most abundant mimicry pattern, COCALA (orange-white banded). Increased rates of mimicry pattern evolution are also found toward the equator. These results underscore the complexity of mimicry evolution in the Neotropical limenitidines i.e., Adelpha and Adelphina, emphasizing the need to explore its interplay with other biotic and abiotic factors.

evolutionary biology↗

bioRxiv2025

Evolution of opsin genes in closely-related species of butterflies specialized in different microhabitats.

How do adaptive processes acting on the coevolution of opsin genes shape the evolution of colour vision in animals? At large phylogenetic scales, natural selection due to the contrasted light environments has been found to impact the evolution of photoreceptor genes. However, in closely-related species, species interactions due to sexual selection or competition may also influence opsin evolution. Here, we investigate the diversification of opsin sequences and their expression in closely-related blue Morpho butterfly species, living in different vertical strata within tropical forests, to shed light on the biotic and abiotic selective pressures shaping the coordinated evolution of opsin genes. We combined comparative genomics, transcriptomics, and immunochemistry to characterize the expression and the spatial distribution of the opsin proteins found in the eyes of Morpho helenor. We detected a double duplication of the LW opsin and found unique ommatidial types compared to other butterfly species. We then investigated the evolution of opsin genes among 21 Morpho species, found signatures of positive selection on two opsin genes (LW3Rh and BRh), and identified key co-evolving amino-acids within and among these two opsin genes. We showed that such opsin evolution was correlated with both light environment and wing coloration, highlighting the joint effect of several selective pressures in the coordinated evolution of proteins.

evolutionary biology↗

bioRxiv2023

Mimetic butterfly wings through mimetic butterfly eyes: Evidence that brightness vision helps Adelpha fessonia identify potential mates

Color vision is thought to play a key role in the evolution of animal coloration, while achromatic vision is rarely considered as a mechanism for species recognition. Here we test the hypothesis that brightness vision rather than color vision helps Adelpha fessonia butterflies identify potential mates while their co-mimetic wing coloration is indiscriminable to avian predators. We examine the trichromatic visual system of A. fessonia and characterize its photoreceptors using RNA-seq, eyeshine, epi- microspectrophotometry and optophysiology. We model the discriminability of its wing color patches in relation to those of its co-mimic, A. basiloides, through A. fessonia and avian eyes. Visual modeling suggests that neither A. fessonia nor avian predators can readily distinguish the co-mimics coloration using chromatic or achromatic vision under natural conditions. These results suggest that mimetic colors are well-matched to visual systems to maintain mimicry, and that mate avoidance between these two look-alike species relies on other cues.

evolutionary biology↗

bioRxiv2021

Multiple mechanisms of photoreceptor spectral tuning following loss of UV color vision in Heliconius butterflies

Color vision modifications occur in animals via a process known as spectral tuning. In Heliconius butterflies, a genus-specific UVRh opsin duplication led to the evolution of UV color discrimination in Heliconius erato females, a rare trait among butterflies. In the H. melpomene and H. ismenius lineages, the UV2 receptor has been lost. Here we compare how loss of the UV2 photoreceptor has altered the visual system of these butterflies. We compare visual system evolution in three Heliconius butterfly species using a combination of intracellular recordings, ATAC-seq, and antibody staining. We identify several spectral tuning mechanisms including adaptive evolution of opsins, deployment of two types of filtering pigments, and co-expression of two distinct opsins in the same cell. Our data show that opsin gain and loss is driving rapid divergence in Heliconius visual systems via tuning of multiple spectral classes of photoreceptor in distinct lineages, potentially contributing to ongoing speciation in this genus.

evolutionary biology↗

bioRxiv2020

True UV color vision in a butterfly with two UV opsins

O_LITrue color vision in animals is achieved when wavelength discrimination occurs based on chromatic content of the stimuli, regardless of intensity. In order to successfully discriminate between multiple wavelengths, animals must use at least two photoreceptor types with different spectral sensitivity peaks. C_LIO_LIHeliconius butterflies have duplicate UV opsin genes, which encode two kinds of photoreceptors with peak sensitivities in the ultraviolet and violet, respectively. In H. erato, the ultraviolet photoreceptor is only expressed in females. C_LIO_LIEvidence from intracellular recordings suggests female H. erato may be able to discriminate between UV wavelengths, however, this has yet to be tested experimentally. C_LIO_LIUsing an arena with a controlled light setting, we tested the ability of H. erato, and two species lacking the violet receptor, H. melpomene and outgroup Eueides isabella, to discriminate between two ultraviolet wavelengths, 380 and 390 nm, as well as two blue wavelengths, 400 and 436 nm, after being trained to associate each stimulus with a food reward. Wavelength stimuli were presented in varying intensities to rule out brightness as a cue. C_LIO_LIWe found that H. erato females were the only butterflies capable of color vision in the UV range; the other butterflies had an intensity-dependent preference for UV stimuli. Across species, both sexes showed color vision in the blue-range. C_LIO_LIModels of H. erato color vision suggest that females have an advantage over males in discriminating the inner UV-yellow corolla of Psiguria pollen flowers from the surrounding outer orange petals, while previous models (McCulloch et al. 2017) suggested that H. erato males have an advantage over females in discriminating Heliconius 3-hyroxykynurenine (3-OHK) yellow wing coloration from non-3-OHK yellow wing coloration found in mimics. C_LIO_LIThese results provide some of the first behavioral evidence for UV color discrimination in Heliconius females in the context of foraging, lending support to the hypothesis (Briscoe et al. 2010) that the duplicated UV opsin genes function together in UV color vision. Taken together, the sexually dimorphic visual system of H. erato appears to have been shaped by both sexual selection and sex-specific natural selection. C_LI

animal behavior and cognition↗

bioRxiv2019

Evolution of Phototransduction Genes in Lepidoptera

Vision is underpinned by phototransduction, a signaling cascade that converts light energy into an electrical signal. Among insects, phototransduction is best understood in Drosophila melanogaster. A survey of phototransduction genes in four insect genomes found gains and losses between D. melanogaster and other insects; this study did not include lepidopterans. Diurnal butterflies and nocturnal moths occupy different light environments and have distinct eye morphologies, which might impact the expression of their phototransduction genes. Here, we used transcriptomics and phylogenetics to identify phototransduction genes that vary between D. melanogaster and Lepidoptera, and between moths and butterflies. Most phototransduction genes were conserved between D. melanogaster and Lepidoptera, with some exceptions. We found two lepidopteran opsins lacking a D. melanogaster ortholog, and using antibodies found that one, a candidate retinochrome which we name unclassified opsin (UnRh), is expressed in the crystaline cone cells and the pigment cells of the butterfly Heliconius melpomene. We also found differences between Lepidoptera and D. melanogaster phototransduction in diacylglycerol regulation where a lepidopteran paralog, DAG{beta}, may be taking on a role in vision. Lastly, butterflies express similar amounts of trp and trpl channel mRNAs, while moths express approximately 50x less trp. Since TRP/TRPL channels allow Ca2+ and Na+ influx this might explain why moths appear to express less Calx and Nckx30C Na+/Ca2+ channel mRNAs. Our findings suggest that while many single-copy D. melanogaster phototransduction genes are conserved in lepidopterans, phototransduction gene expression differences exist between moths and butterflies that may be linked to their visual light environment.

evolutionary biology↗

bioRxiv2018

Drift and directional selection are the evolutionary forces driving gene expression divergence in eye and brain tissue of Heliconius butterflies

Investigating gene expression evolution over micro- and macroevolutionary timescales will expand our understanding of the role of gene expression in adaptation and speciation. In this study, we characterized which evolutionary forces are acting on gene expression levels in eye and brain tissue of five Heliconius butterflies with divergence times of ~5-12 MYA. We developed and applied Brownian motion and Ornstein-Uhlenbeck models to identify genes whose expression levels are evolving through drift, stabilizing selection, or a lineage-specific shift. We find that 81% of the genes evolve under genetic drift. When testing for branch-specific shifts in gene expression, we detected 368 (16%) shift events. Genes showing a shift towards up-regulation have significantly lower gene expression variance than those genes showing a shift leading towards down-regulation. We hypothesize that directional selection is acting in shifts causing up-regulation, since transcription is costly. We further uncover through simulations that parameter estimation of Ornstein-Uhlenbeck models is biased when using small phylogenies and only becomes reliable with phylogenies having at least 50 taxa. Therefore, we developed a new statistical test based on Brownian motion to identify highly conserved genes (i.e., evolving under strong stabilizing selection), which comprised 3% of the orthoclusters. In conclusion, we found that drift is the dominant evolutionary force driving gene expression evolution in eye and brain tissue in Heliconius. Nevertheless, the higher proportion of genes evolving under directional than under stabilizing selection might reflect species-specific selective pressures on vision and brain necessary to fulfill species-specific requirements.

evolutionary biology↗

bioRxiv2016

Ultraviolet and yellow reflectance but not fluorescence is important for visual discrimination of conspecifics by Heliconius erato

Toxic Heliconius butterflies have yellow hindwing bars that - unlike their closest relatives - reflect ultraviolet (UV) and long wavelength light, and also fluoresce. The pigment in the yellow scales is 3-hydroxy-DL-kynurenine (3-OHK), found also in the hair and scales of a variety of animals. In other butterflies including pierids, which similarly display wing colors that vary in both the UV and the human-visible range, behavioral experiments have indicated that only the UV component is most relevant to mate choice. Whether in Heliconius butterflies it is the UV, the human-visible yellow, and/or the fluorescent component of yellow wing coloration that is relevant to mate choice is unknown. In field studies with butterfly paper models we show that both UV and 3-OHK yellow act as signals for H. erato but attack rates by birds do not differ significantly between the models. Furthermore, measurement of the quantum yield and reflectance spectra of 3-OHK indicates that fluorescence does not contribute to the visual signal under broad-spectrum illumination. Our results suggest that the use of 3-OHK pigmentation instead of ancestral yellow was driven by sexual selection rather than predation.\n\nSummary statementHeliconius butterflies use a co-opted yellow pigment for communication, while predators are fooled by non-Heliconius mimics using ancestral yellow pigments.

animal behavior and cognition↗