Biology subjects

Counterman, B. A.

Publications and source records attributed to Counterman, B. A..

6 recordsLinked to original sources

bioRxiv2022

Seasonal polyphenism of wing colors and its influence on sulphur butterfly diversification

Seasonal variation of color patterns on butterfly wings are iconic examples of developmentally plastic traits that can influence adaptation and speciation. Yet, there are few examples of such seasonal polyphenisms that have characterized the environmental cues, ecological consequences, or genetic mechanisms involved in generating the plastic variation of wing color. Further, there is a lack of support that such plasticity may impact the adaptive diversification of butterfly wing patterns. Here, we report a case of seasonal polyphenism in pigment and structurally-based color patterns of Zerene cesonia that are strikingly similar to the color pattern divergence seen on the wings of sulphur butterflies. We show that (i) coordinated changes in temperature and photoperiod drive the plasticity, (ii) the plastic color changes impact how fast the butterflies can warm, (iii) identify spalt as likely be involved in the genetic coupling of the pigment and structurally-based color plastic response. We further show that this plastic wing changes phenocopy wing pattern divergence between Zerene species, as well as the color pattern differences known to be commonly involved in sexual selection and speciation across sulphur butterflies. Together, our results demonstrate that shared environmental cues and genetic basis for pigment and structural color plasticity may result in conditions that may have facilitated species diversification of sulphur butterflies.

evolutionary biology↗

bioRxiv2022

A butterfly pan-genome reveals a large amount of structural variation underlies the evolution of chromatin accessibility

Despite insertions and deletions being the most common structural variants (SVs) found across genomes, not much is known about how much these SVs vary within populations and between closely related species, nor their significance in evolution. To address these questions, we characterized the evolution of indel SVs using genome assemblies of three closely related Heliconius butterfly species. Over the relatively short evolutionary timescales investigated, up to 18.0% of the genome was composed of indels between two haplotypes of an individual H. charithonia butterfly and up to 62.7% included lineage-specific SVs between the genomes of the most distant species (11 Mya). Lineage-specific sequences were mostly characterized as transposable elements (TEs) inserted at random throughout the genome and their overall distribution was similarly affected by linked selection as single nucleotide substitutions. Using chromatin accessibility profiles (i.e., ATAC-seq) of head tissue in caterpillars to identify sequences with potential cis-regulatory function, we found that out of the 31,066 identified differences in chromatin accessibility between species, 30.4% were within lineage-specific SVs and 9.4% were characterized as TE insertions. These TE insertions were localized closer to gene transcription start sites than expected at random and were enriched for several transcription factor binding site candidates with known function in neuron development in Drosophila. We also identified 24 TE insertions with head-specific chromatin accessibility. Our results show high rates of structural genome evolution that were previously overlooked in comparative genomic studies and suggest a high potential for structural variation to serve as raw material for adaptive evolution.

genomics↗

bioRxiv2021

A genetic switch for male UV-iridescence in an incipient species pair of sulphur butterflies

Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of UV iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern US with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X (or large-Z) effect. Within this chromosome-wide reproductive barrier, linkage mapping indicates that cis-regulatory variation of bric a brac (bab) underlies the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knock-out, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results highlight how a genetic switch can regulate a premating signal and integrate with other reproductive barriers during intermediate phases of speciation. Significance statementIncipient species are at an intermediate stage of speciation where reproductive isolation is counteracted by the homogenizing effects of gene flow. Human activity sometimes leads such species to reunite, as seen in the Orange Sulphur butterfly, which forms large hybridizing populations with the Clouded Sulphur in alfalfa fields. Here we show that the sex chromosome maintains these species as distinct, while the rest of their genome is admixed. Sex chromosomes notably determine which males display to females a bright, iridescent ultraviolet signal on their wings. Genetic mapping, antibody stainings, and CRISPR knock-outs collectively indicate that the gene bric a brac controls whether UV-iridescent nanostructures develop in each species, elucidating how a master switch gene modulates a male courtship signal.

evolutionary biology↗

bioRxiv2020

Selection and gene flow define polygenic barriers between incipient butterfly species

Characterizing the genetic architecture of species boundaries remains a difficult task. Hybridizing species provide a powerful system to identify the factors that shape genomic variation and, ultimately, identify the regions of the genome that maintain species boundaries. Unfortunately, complex histories of isolation, admixture and selection can generate heterogenous genomic landscapes of divergence which make inferences about the regions that are responsible for species boundaries problematic. However, as the signal of admixture and selection on genomic loci varies with recombination rate, their relationship can be used to infer their relative importance during speciation. Here, we explore patterns of genomic divergence, admixture and recombination rate among hybridizing lineages across the Heliconius erato radiation. We focus on the incipient species, H. erato and H. himera, and distinguish the processes that drive genomic divergence across three contact zones where they frequently hybridize. Using demographic modeling and simulations, we infer that periods of isolation and selection have been major causes of genome-wide correlation patterns between recombination rate and divergence between these incipient species. Upon secondary contact, we found surprisingly highly asymmetrical introgression between the species pair, with a paucity of H. erato alleles introgressing into the H. himera genomes. We suggest that this signal may result from a current polygenic species boundary between the hybridizing lineages. These results contribute to a growing appreciation for the importance of polygenic architectures of species boundaries and pervasive genome-wide selection during the early stages of speciation with gene flow.

evolutionary biology↗

bioRxiv2020

Perfect mimicry between Heliconius butterflies is constrained by genetics and development

Mullerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. The butterfly species Heliconius erato and Heliconius melpomene have a large diversity of co-mimicking geographic races with remarkable resemblance in melanic patterning across the mid-forewing that has been linked to expression patterns of the gene WntA. Recent CRISPR/Cas9 experiments have informed us on the exact areas of the wings in which WntA affects color pattern formation in both H. erato and H. melpomene, thus providing a unique comparative dataset to explore the functioning of a gene and its potential effect on phenotypic evolution. We therefore quantified wing color pattern differences in the mid-forewing region of 14 co-mimetic races of H. erato and H. melpomene and measured the extent to which mimicking races are not perfectly identical. While the relative size of the mid-forewing pattern is generally nearly identical, our results highlight the areas of the wing that prevent these species from achieving perfect mimicry and demonstrate that this mismatch can be largely explained by constraints imposed by divergence in the gene regulatory network that define wing color patterning. Divergence in the developmental architecture of a trait can thus constrain morphological evolution even between relatively closely related species.

evolutionary biology↗

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↗