Biology subjects

Martin, S. H.

Publications and source records attributed to Martin, S. H..

At least 19 recordsLinked to original sources

bioRxiv2025

A model-free method for genealogical inference without phasing and its application for topology weighting

Recent advances in methods to infer and analyse ancestral recombination graphs (ARGs) are providing powerful new insights in evolutionary biology and beyond. Existing inference approaches tend to be designed for use with fully-phased datasets, and some rely on model assumptions about demography and recombination rate. Here I describe a simple model-free approach for genealogical inference along the genome from unphased genotype data called Sequential Tree Inference by Collecting Compatible Sites (sticcs). sticcs applies a heuristic algorithm based on the perfect phylogeny principle to reconstruct a local genealogy at each variant site in the genome, using a collecting procedure to import information from other nearby sites. Using simulations, I show that sticcs is accurate for ARG inference, but only when the sample size is small. However, I also describe how it can be applied for the purpose of topology weighting by stacking tree sequences inferred for multiple subsets of the data, removing the sample size restriction. Topology weights estimated in this way from unphased data tend to be more accurate than those computed with full ARGs inferred from perfectly phased data using several popular tools. The methods presented therefore have promise for analysis of relatedness and introgression in non-model species, including polyploids. The new methods are implemented in two Python packages, sticcs (for ARG inference) and twisst2 (for topology weighting using the stacking procedure), which both interface with the tskit library for analysis of tree sequence objects.

genomics↗

bioRxiv2024

Introgression and divergence in a young species group

The process of speciation concerns often not only pairs of species but rather groups of diverging and interacting taxa, as highlighted by recent research. Hence, to understand the evolution of species diversity and their persistence, it is crucial to understand how gene flow and evolution of reproductive isolation shape groups of closely related species. Using resequencing data, we disentangle here genomic patterns of divergence and introgression in five Formica rufa group wood ant species that are at the early stage of speciation. We first revise earlier mitochondrial phylogenies with a nuclear genomic tree, and demonstrate then introgression that is in line with observations of their current day natural hybridisation. Investigating the genome-wide differentiation and divergence we find correlations between population genetic parameters of divergence, differentiation, and diversity, that are in line with theoretical expectations for young species. Despite previously found evidence for polygenic species barriers, our data lacks the genome-wide correlation between differentiation and divergence that would be expected under a model of polygenic barriers. The likely explanation for this lack is the dominating effect of ancestral diversity at these early stages of speciation. As hybridisation has led to both deleterious and adaptive consequences within the group, we examined the signatures of introgression. We find no strong positive correlation between introgression and recombination, suggesting introgression does not have a predominantly deleterious effect. We also infer low diversity in the genomic regions with high proportions of introgression, consistent with the idea that selection has locally favoured introgression. This could be due to sharing of adaptive alleles or reduction of genetic load in the receiving species. Interestingly, gene flow in this group could potentially cross multiple species boundaries even in the absence of direct interbreeding between all the species. We discuss the long-term benefits and costs of introgression in young species, including the effect of environmental fluctuations and multi-species introgression.

evolutionary biology↗

bioRxiv2024

Extensive haplotype diversity in a butterfly colour pattern supergene is fuelled by incomplete recombination suppression

Supergenes can evolve when recombination-suppressing mechanisms like inversions promote co-inheritance of alleles at two or more polymorphic loci that affect a complex trait. Theory shows that such genetic architectures can be favoured under balancing selection or local adaptation in the face of gene flow, but they can also bring costs associated with reduced opportunities for recombination. These costs may in turn be offset by rare gene flux between inverted and ancestral haplotypes, with a range of possible outcomes. We aimed to shed light on these processes by investigating the BC supergene, a large genomic region comprising multiple rearrangements associated with three distinct wing color morphs in Danaus chrysippus, a butterfly known as the African monarch, African queen and plain tiger. Using whole-genome resequencing data from 174 individuals, we first confirm the effects of BC on wing color pattern: background melanism is associated with SNPs in the promoter region of yellow, within an inverted subregion of the supergene, while forewing tip pattern is most likely associated with copy number variation in a separate subregion of the supergene. We then show that haplotype diversity within the supergene is surprisingly extensive: there are at least six divergent haplotype groups that experience suppressed recombination with respect to each other. Despite high divergence between these haplotype groups, we identify an unexpectedly large number of natural recombinant haplotypes. Several of the inferred crossovers occurred between adjacent inversion modules, while others occurred within inversions. Furthermore, we show that new haplotype groups have arisen through recombination between two pre-existing ones. Specifically, an allele for dark coloration in the promoter of yellow has recombined into distinct haplotype backgrounds on at least two separate occasions. Overall, our findings paint a picture of dynamic evolution of supergene haplotypes, fuelled by incomplete recombination suppression.

evolutionary biology↗

bioRxiv2024

A novel ClpC adaptor protein that functions in the developing Bacillus subtilis spore

Bacterial protein degradation machinery consists of chaperone-protease complexes that play vital roles in bacterial growth and development and have sparked interest as novel antimicrobial targets. ClpC-ClpP (ClpCP) is one such chaperone-protease, recruited by adaptors to specific functions in the model bacterium Bacillus subtilis and other Gram-positive bacteria including the pathogens Staphylococcus aureus and Mycobacterium tuberculosis. Here we have identified a new ClpCP adaptor protein, MdfA ("Metabolic differentiation factor A", formerly YjbA), in a genetic screen for factors that help drive B. subtilis toward metabolic dormancy during spore formation. A knockout of mdfA stimulates gene expression in the developing spore, while aberrant expression of mdfA during vegetative growth is toxic. MdfA binds directly to ClpC to induce its oligomerization and ATPase activity, and this interaction is required for the in vivo effects of mdfA. Finally, a co-crystal structure reveals that MdfA binds to the ClpC N-terminal domain at a location analogous to that on the M. tuberculosis ClpC1 protein where bactericidal cyclic peptides bind. Altogether our data and that of an accompanying study by Riley, Lyda and colleagues support a model in which MdfA induces ClpCP-mediated degradation of metabolic enzymes in the developing spore, helping drive it toward metabolic dormancy.

microbiology↗

bioRxiv2023

Inferring inter-chromosomal rearrangements and ancestral linkage groups from synteny

Chromosome rearrangements shape the structure of the genome and influence evolutionary processes. Inferring ancestral chromosomes and rearrangements across a phylogenetic tree is therefore an important analysis within evolutionary genetics. One approach to this inference problem is to focus on synteny information, i.e. the co-occurrence of loci on the same chromosome. Although algorithms for inferring ancestral linkage groups (ALGs) and inter-chromosomal rearrangements from synteny have been previously described, they have seldom been applied to modern genome data. Here we implement these algorithms in a command-line tool, syngraph, and evaluate their performance using simulations that include a mix of different rearrangements and types of error. We show that ALGs and rearrangements can be recovered when the rearrangement frequency per-branch is well below the number of chromosomes. We demonstrate that competing models of rearrangement can be inferred by comparing observed results to simulations. Finally, we reanalyse genome assemblies of rhabditid nematodes and find that independent fusions of the same ALGs pose a challenge that is difficult to overcome without gene-order information. Our simulations and analysis of real data demonstrate both the promise and limitations of using synteny information to infer patterns of genome evolution.

evolutionary biology↗

bioRxiv2023

Transposable element insertions are associated with Batesian mimicry in the pantropical butterfly Hypolimnas misippus

Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate the four colour morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved a wing pattern present in other Hypolimnas species for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, we discover two large transposable element (TE) insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing the ancestral and mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that the TEs disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.

evolutionary biology↗

bioRxiv2023

Do chromosome rearrangements fix by genetic drift or natural selection? A test in Brenthis butterflies

Large-scale chromosome rearrangements, such as fissions and fusions, are a common feature of eukaryote evolution. They can have considerable influence on the evolution of populations, yet it remains unclear exactly how rearrangements become established and eventually fix. Rearrangements could fix by genetic drift if they are weakly deleterious or neutral, or they may instead be favoured by positive natural selection. Here we compare genome assemblies of three closely related Brenthis butterfly species and characterise a complex history of fission and fusion rearrangements. An inferred demographic history of these species suggests that rearrangements became fixed in populations with large long-term effective size (Ne). However, we also find large runs of homozygosity within individual genomes and show that a model of population structure with smaller local Ne can reconcile these observations. Using a recently developed analytic framework for characterising hard selective sweeps, we find that chromosome fusions are not enriched for evidence of past sweeps compared to other regions of the genome. Nonetheless, one chromosome fusion in the B. daphne genome is associated with a valley of diversity where genealogical branch lengths are distorted, consistent with a selective sweep. Our results suggest that drift is a stronger force in these populations than suggested by overall genetic diversity, but that the fixation of strongly underdominant rearrangements remains unlikely. Additionally, although chromosome fusions do not typically exhibit signatures of selective sweeps, a single example raises the possibility that natural selection may sometimes play a role in their fixation.

evolutionary biology↗

bioRxiv2023

The Hypolimnas misippus genome supports a common origin of the W chromosome in Lepidoptera

Moths and butterflies (Lepidoptera) have a heterogametic sex chromosome system with females carrying ZW chromosomes and males ZZ. The lack of W chromosomes in early diverging lepidopteran lineages has led to the suggestion of an ancestral Z0 system in this clade and a B chromosome origin of the W. This contrasts with the canonical model of W chromosome evolution in which the W would have originated from the same homologous autosomal pair as the Z chromosome. Despite the distinct models proposed, the rapid evolution of the W chromosome has hindered the elucidation of its origin. Here, we present high-quality, chromosome-level genome assemblies of two Hypolimnas species (Hypolimnas missipus and Hypolimnas bolina) and use the H. misippus assembly to explore the evolution of W chromosomes in butterflies and moths. We show that in H. misippus the W chromosome has higher similarity to the Z chromosome than any other chromosome, which could suggest a possible origin from the same homologous autosome pair as the Z chromosome. However, using genome assemblies of closely related species (ditrysian lineages) containing assembled W chromosomes, we present contrasting evidence suggesting that the W chromosome might have evolved from a B chromosome instead. Crucially, by using a synteny analysis to infer homology, we show that W chromosomes are likely to share a common evolutionary origin in Lepidoptera. This study highlights the difficulty of studying the evolution of W chromosomes and contributes to better understanding its evolutionary origins. SignificanceButterflies and moths have a sex determination system in which females carry two different sex chromosomes, Z and W, while males carry two copies of the Z. The evolutionary origin of the W chromosome has been elusive, with many possible scenarios being suggested, such as the independent evolution of W chromosomes in many butterfly and moth species. Here, we present genome assemblies of two Hypolimnas butterfly species and use one of them to shed light on the evolution of the W chromosome. We show that W chromosomes across butterflies and moths are very similar which suggests a shared common origin.

genomics↗

bioRxiv2023

Genome sequence of Ophryocystis elektroscirrha, an apicomplexan parasite of monarch butterflies: cryptic diversity and response to host-sequestered plant chemicals

Apicomplexa are ancient and diverse organisms which have been poorly characterized by modern genomics. To better understand the evolution and diversity of these single-celled eukaryotes, we sequenced the genome of Ophryocystis elektroscirrha, a parasite of monarch butterflies, Danaus plexippus. The genome is miniscule, totaling only 9 million bases and containing fewer than 3,000 genes. We then compared this new sequence to the two other sequenced invertebrate-infecting apicomplexans, Porospora gigantea and Gregarina niphandrodes, which have nearly twice the gene content and found that O. elektroscirrha shares different orthologs with each sequenced relative, suggesting the true set of universally conserved apicomplexan genes is very small indeed. We investigated sequenced reads from other potential hosts to explore the viability of in silico infection screening. We recovered a similarly sized parasite genome from another butterfly, Danaus chrysippus, that was highly diverged from the O. elektroscirrha reference, possibly representing a distinct species. Using these two new genomes, we investigated potential evolutionary response by parasites to toxic phytochemicals their hosts ingest and sequester. Monarch butterflies are well-known to tolerate toxic cardenolides thanks to changes in the sequence of their Type II ATPase sodium pumps. We show that Ophryocystis completely lacks Type II or Type 4 sodium pumps, and related proteins PMCA calcium pumps show extreme sequence divergence compared to other Apicomplexa, demonstrating new avenues of research opened by genome sequencing of non-model Apicomplexa. Author SummaryThere are many relatives of Plasmodium, the single-celled parasites responsible for malaria, and they infect a wide range of animals, including insects. These parasites have received less attention however, leaving much unknown about them. We sequenced the genome of one such parasite, Ophryocystis elektroscirrha (OE), to compare it to better-studied parasites and shed light on OEs interaction with its host, the monarch butterfly. We found that OE has a tiny genome with the fewest genes of any sequenced parasite in this group, lacking many genes found in its relatives. Using our new data, we also discovered evidence that infections of other butterfly species that have been attributed to OE may be caused by a previously undiscovered distinct parasite species. And finally, we explored the evolution of a family of genes that may be targeted by medicinal plant compounds in the monarch butterflys diet; OE has lost one of these genes and radically changed the sequence of another, setting a direction for future research.

genomics↗

bioRxiv2022

Subtle introgression footprints at the end of the speciation continuum in a clade of Heliconius butterflies

Quantifying gene flow between lineages at different stages of the speciation continuum is central to understanding speciation. Heliconius butterflies have undergone an adaptive radiation in wing colour patterns driven partly by natural selection for local mimicry. Colour patterns are also known to be used as assortative mating cues. Therefore, wing pattern divergence is considered to play a role in speciation. A corollary is that mimicry between closely-related species may be associated with hybridization and interfere with reproductive isolation. Here, we take a multifaceted approach to explore speciation history, species boundaries, and traits involved in species differentiation between the two closely-related species H. hecale and H. ismenius. We focus on geographic regions where the two species mimic each other, and contrast this with geographic regions where they do not mimic each other. To examine population history and patterns of gene flow, we tested and compared a four-population model accounting for linked selection. This model suggests that the two species have remained isolated for a large part of their history, yet with a small amount of gene exchange. Accordingly, signatures of genomic introgression were small except at a major wing pattern allele and chemosensing genes, and stronger in the mimetic populations compared to non-mimetic populations. Behavioural assays confirm that visual confusion exists but that short-range cues determine strong sexual isolation. Tests for chemical differentiation between species identified major differences in putative pheromones which likely mediate mate choice and the maintenance of species differences.

evolutionary biology↗

bioRxiv2022

Recent evolution of a maternally-acting sex-determining supergene in a fly with single-sex broods

Sex determination is a key developmental process, yet it is remarkably variable across the tree of life. The dipteran family Sciaridae exhibits one of the most unusual sex determination systems in which mothers control offspring sex through selective elimination of paternal X chromosomes. Whereas in some members of the family females produce mixed-sex broods, others such as the dark-winged fungus gnat Bradysia coprophila are monogenic, with females producing single-sex broods. Female-producing females were previously found to be heterozygous for a large X-linked paracentric inversion (X), which is maternally inherited and absent from male-producing females. Here we assembled and characterized the X sequence. As close sequence homology between the X and X made identification of the inversion challenging, we developed a k-mer-based approach to bin genomic reads before assembly. We confirmed that the inversion spans most of the X chromosome (approximately 55Mb) and encodes around 3500 genes. Analysis of the divergence between the inversion and the homologous region of the X revealed that it originated very recently (<0.5 mya). Surprisingly, we found that the X is more complex than previously thought and is likely to have undergone multiple rearrangements that have produced regions of varying ages, resembling a supergene composed of evolutionary strata. We found functional degradation of around 7.3% of genes within the region of recombination suppression, but no evidence of accumulation of repetitive elements. Our findings provide an indication that sex-linked inversions are driving turnover of the strange sex determination system in this family of flies.

evolutionary biology↗

bioRxiv2022

Chromosome fissions and fusions act as barriers to gene flow between Brenthis fritillary butterflies

Chromosome rearrangements are thought to promote reproductive isolation between incipient species. However, it is unclear how often, and under what conditions, fission and fusion rearrangements act as barriers to gene flow. Here we investigate speciation between two largely sympatric fritillary butterflies, Brenthis daphne and B. ino. We use a composite likelihood approach to infer the demographic history of these species from whole genome sequence data. We then compare chromosome-level genome assemblies of individuals from each species and identify a total of nine chromosome fissions and fusions. Finally, we fit a demographic model where effective population sizes and effective migration rate vary across the genome, allowing us to quantify the effects of chromosome rearrangements on reproductive isolation. We show that chromosomes involved in rearrangements experienced less effective migration since the onset of species divergence and that genomic regions near rearrangement points have a further reduction in effective migration rate. Our results suggest that the evolution of multiple rearrangements in the B. daphne and B. ino populations, including alternative fusions of the same chromosomes, have resulted in a reduction in gene flow. While fission and fusion of chromosomes are unlikely to be the only processes that have led to speciation between these butterflies, this study shows that these rearrangements can directly promote reproductive isolation and may be involved in speciation when karyotypes evolve quickly.

evolutionary biology↗

bioRxiv2022

Demographically explicit scans for barriers to gene flow using gIMble

Identifying regions of the genome that act as barriers to gene flow between recently diverged taxa has remained challenging given the many evolutionary forces that generate variation in genetic diversity and divergence along the genome, and the stochastic nature of this variation. Progress has been impeded by a conceptual and methodological divide between analyses that infer the demographic history of speciation and genome scans aimed at identifying locally maladaptive alleles i.e. genomic barriers to gene flow. Here we implement genomewide IM blockwise likelihood estimation (gIMble), a composite likelihood approach for the quantification of barriers, that bridges this divide. This analytic framework captures background selection and selection against barriers in a model of isolation with migration (IM) as heterogeneity in effective population size (Ne) and effective migration rate (me), respectively. Variation in both effective demographic parameters is estimated in sliding windows via pre-computed likelihood grids. gIMble includes modules for pre-processing/filtering of genomic data and performing parametric bootstraps using coalescent simulations. To demonstrate the new approach, we analyse data from a well-studied pair of sister species of tropical butterflies with a known history of post-divergence gene flow: Heliconius melpomene and H. cydno. Our analyses uncover both large-effect barrier loci (including well-known wing-pattern genes) and a genome-wide signal of a polygenic barrier architecture. Author summaryAs a fundamental process generating biological diversity, speciation involves the evolution of reproductive isolation and thus the build-up of barriers to genetic exchange among organismal groups. While population genomic data are arguably the only source of information we have about most recent speciation events, the way such data are analysed remains depressingly superficial: population genomic studies of speciation are phrased either as scans for outliers of genetic differentiation, or are based on models of neutral evolution under the constraint of a single genome-wide demography. Here we introduce a new statistical framework called gIMble to estimate the effective rate of gene flow and the effective population sizes along the genome from population genomic data. By capturing genome-wide variation in these two effective demographic parameters, gIMble disentangles the genomic footprints of different modes of selection and provides a direct quantification of the species barrier. To illustrate this framework, we analyse a classic speciation genomic dataset from Heliconius butterflies. We show that barriers to gene flow in this system include both large effect loci - most, but not all, of which were known from functional work - as well as a genome-wide signature of weak-effect polygenic barriers.

evolutionary biology↗

bioRxiv2022

Rapid and repeatable genome evolution across three hybrid ant populations

Hybridization is frequent in the wild but it is unclear whether admixture events lead to predictable outcomes and if so, at what timescale. We show that selection led to correlated sorting of genetic variation in less than 50 generations in three hybrid Formica aquilonia x F. polyctena ant populations. Removal of ancestry from the species with the lowest effective population size happened repeatedly in all populations, consistent with purging of deleterious load. This process was modulated by recombination rate variation and the density of functional sites. Moreover, haplotypes with signatures of positive selection in either species were more likely to fix in hybrids. These mechanisms led to mosaic genomes with comparable ancestry proportions. Our work demonstrates predictable evolution over short timescales after admixture in nature.

evolutionary biology↗

bioRxiv2021

Stepwise evolution of a butterfly supergene via duplication and inversion

Supergenes maintain adaptive clusters of alleles in the face of genetic mixing. Although usually attributed to inversions, supergenes can be complex, and reconstructing the precise processes that led to recombination suppression and their timing is challenging. We investigated the origin of the BC supergene, which controls variation in warning colouration in the African Monarch butterfly, Danaus chrysippus. By generating chromosome-scale assemblies for all three alleles, we identified multiple structural differences. Most strikingly, we find that a region of >1 million bp underwent several segmental duplications at least 7.5 million years ago. The resulting duplicated fragments appear to have triggered four inversions in surrounding parts of the chromosome, resulting in stepwise growth of the region of suppressed recombination. Phylogenies for the inversions are incongruent with the species tree, and suggest that structural polymorphisms have persisted for at least 4.1 million years. In addition to the role of duplications in triggering inversions, our results suggest a previously undescribed mechanism of recombination suppression through independent losses of divergent duplicated tracts. Overall, our findings add support for a stepwise model of supergene evolution involving a variety of structural changes.

evolutionary biology↗

bioRxiv2021

Repeated genetic adaptation to high altitude in two tropical butterflies

Repeated evolution can provide insight into the mechanisms that facilitate adaptation to novel or changing environments. Here we study adaptation to high altitude in two divergent tropical butterflies, H. erato and H. melpomene, which have repeatedly and independently adapted to high elevations on either side of the Andean mountains. We sequenced 518 whole genomes from elevational transects and found many regions under selection at high altitude, with repeated genetic differentiation across multiple replicates, including allopatric comparisons. In contrast, there is little molecular parallelism between H. erato and H. melpomene. With a further 85 whole genomes of five close relatives, we find that a large proportion divergent regions have arisen from standing variation and putative adaptive introgression from high-altitude specialist species. Taken together our study supports a key role of standing genetic variation and gene flow from pre-adapted species in promoting parallel genetic local adaptation to the environment.

evolutionary biology↗

bioRxiv2021

Genome assembly of Danaus chrysippus and comparison with the Monarch Danaus plexippus

Milkweed butterflies in the genus Danaus are studied in a diverse range of research fields including the neurobiology of migration, biochemistry of plant detoxification, host-parasite interactions, evolution of sex chromosomes, and speciation. We have assembled a nearly chromosomal genome for Danaus chrysippus (known as the African Monarch, African Queen, and Plain Tiger) using long read sequencing data. This species is of particular interest for the study of genome structural change and its consequences for evolution. Comparison with the genome of the North American Monarch Danaus plexippus reveals generally strong synteny, but highlights three inversion differences. The three chromosomes involved were previously found to carry peaks of intra-specific differentiation in D. chrysippus in Africa, suggesting that these inversions may be polymorphic and associated with local adaptation. The D. chrysippus genome is over 40% larger than that of D. plexippus, and nearly all of the additional [~]100 Megabases of DNA comprises repeats. Future comparative genomic studies within this genus will shed light on the evolution of genome architecture.

genomics↗

bioRxiv2021

The effects of chromosome fusions on genetic diversity and evolutionary turnover of functional loci consistently depends on chromosome size

Major changes in chromosome number and structure are linked to a series of evolutionary phenomena, including intrinsic barriers to gene flow or suppression of recombination due to chromosomal rearrangements. However, chromosome rearrangements can also affect the fundamental dynamics of molecular evolution within populations by changing relationships between linked loci and altering rates of recombination. Here, we build chromosome-level assembly Eueides isabella and, together with the chromosome-level assembly of Dryas iulia, examine the evolutionary consequences of multiple chromosome fusions in Heliconius butterflies. These assemblies pinpoint fusion points on 10 of the 21 autosomal chromosomes and reveal striking differences in the characteristics of fused and unfused chromosomes. The ten smallest autosomes in D. iulia and E. isabella, which have each fused to a longer chromosome in Heliconius, have higher repeat and GC content, and longer introns than predicted by their chromosome length. Following fusion, these characteristics change to become more in line with chromosome length. The fusions also led to reduced diversity, which likely reflects increased background selection and selection against introgression between diverging populations, following a reduction in per-base recombination rate. We further show that chromosome size and fusion impact turnover rates of functional loci at a macroevolutionary scale. Together these results provide further evidence that chromosome fusion in Heliconius likely had dramatic effects on population level processes shaping rates of neutral and adaptive divergence. These effects may have impacted patterns of diversification in Heliconius, a classic example of an adaptive radiation.

evolutionary biology↗