Biology subjects

Brelsford, A.

Publications and source records attributed to Brelsford, A..

13 recordsLinked to original sources

bioRxiv2026

Gene flux drives functional changes in an ancient supergene in Formica lemani

Pinpointing the genetic elements underlying a phenotype within a supergene can be difficult because hundreds of linked genes can show similar associations with phenotype. Rare recombination between supergene haplotypes can help identify those genetic elements by changing haplotype-phenotype combinations. Here we investigate the genetic underpinnings of colony queen number and body size in the ant Formica lemani. Throughout the Formica genus, single-queen colonies typically carry M haplotypes, while multi-queen colonies also carry P haplotypes. In F. lemani, we found two P haplotypes homologous to those described in the closely related F. cinerea, but unlike in F. cinerea, where P1 is restricted to multi-queen colonies, F. lemani P1 is common in both single- and multi-queen colonies. This deviation suggests that P1 may carry novel SNP combinations allowing single queen colony compatibility. By comparing haplotypes within F. lemani and with Formica cinerea, we searched for candidate monogyny variants resulting from gene flux from the M onto the P1 haplotype, or with P1-specific mutations. We found 82 genes associated with candidate variants, of which two are among the fourteen previously suggested candidates in other species, suggesting that several different genes may underlie queen number across the genus. We also identified a supergene associated with smaller queens and males, which is shared with F. cinerea and in interchromosomal linkage disequilibrium with the queen-number supergene. Together, these results provide a rare example of how an ancient supergene can change in function, and a step toward identifying the genes within a supergene responsible for its functions.

evolutionary biology↗

bioRxiv2026

Beyond queen number: two supergenes coordinate dispersal, mating, and colony founding in the ant Formica cinerea

Reproductive success often depends on coordinated combinations of morphology, dispersal ability, and mating behavior. Supergenes, genomic regions of suppressed recombination, allow such combinations to be inherited by offspring as a single unit. In ants, independently evolved supergenes control colony queen number, yet few studies have investigated their joint influence on morphology, mating, and colony-founding in sexuals. Formica cinerea provides a unique opportunity to address this question because it harbors two supergenes that together produce three queen and male morphs: large monogyne, large polygyne, and small polygyne. Here we show that these supergenes jointly shape an integrated suite of traits across the reproductive cycle. Wing area was primarily associated with the chromosome 3 supergene, with monogyne individuals having larger wings than polygyne individuals. Thorax volume was associated with the chromosome 9 supergene, with small polygyne individuals having reduced thorax volume regardless of social origin. Mating was assortative for both supergenes in large morphs but random in small polygyne queens. Independent colony founding was almost exclusively performed by large monogyne queens; initial egg production was unaffected by mate genotype. These findings show that the two supergenes jointly coordinate dispersal morphology, mate choice, and colony-founding into coherent reproductive strategies, preventing maladaptive intermediate phenotypes.

evolutionary biology↗

bioRxiv2026

Lethal epistasis maintains strong linkage disequilibrium between unlinked supergenes

Linkage disequilibrium (LD) between adaptive gene combinations is typically maintained through physical linkage and suppressed recombination. Although epistatic interactions can maintain LD between unlinked loci, this mechanism is rarely documented in nature. Supergenes, regions of suppressed recombination containing tightly linked loci, typically exemplify the first mechanism, in which genomic rearrangements lock together coadapted alleles. Here, we demonstrate a rare case of epistasis-driven LD between two supergenes on different chromosomes in the European ant Formica cinerea: one controlling colony queen number (chromosome 3) and another determining sexual body size (chromosome 9). We show that these supergenes assort independently according to Mendelian expectations during meiosis, yet exhibit high LD between the multi-queen haplotype P2 and the miniaturizing haplotype 9r, with small queens and males occurring exclusively in multi-queen colonies. Mismatched genotype combinations (P2 without 9r and vice versa) are severely underrepresented among all adult castes, with mismatched males experiencing complete mortality. We show that this pattern cannot be explained by meiotic drive or maternal-effect killing, assortative mating, or extrinsic selection on adults, indicating strong postzygotic epistatic selection maintaining the observed LD. The fitness costs of these epistatic interactions are substantial but critically depend on mating combinations: heterozygous small queens achieve 1.5-2.5 times higher fitness (based on offspring genotype viability) when mated to small males (P2-9r) compared to large males. Our findings provide empirical evidence for epistatic interactions between unlinked supergenes maintaining LD in the absence of physical linkage.

evolutionary biology↗

bioRxiv2026

Non-canonical sex chromosome evolution revealed by extreme heterogeneity in homomorphic Y chromosome differentiation in the common frog

Sex chromosome evolution is often viewed as a unidirectional process in which recombination suppression expands around a sex-determining locus, leading eventually to Y-chromosome degeneration. Yet many vertebrates, including frogs, retain homomorphic sex chromosomes and polymorphic differentiation despite long-term recombination suppression, which is quite puzzling. Here, we combine pooled whole-genome resequencing, doubled-haploid YY genomes, and RNA-seq to understand the dynamics of homomorphic sex chromosome evolution in a Swiss Alpine population of the common frog, Rana temporaria, where multiple Y haplotypes coexist. We show that two fully differentiated Y haplotypes carry exceptionally large nonrecombining regions spanning [~]90% of the sex chromosome ([~]618-625 Mb), whereas semi-differentiated Y haplotype retains only a 4.64 Mb Dmrt1-linked sex-determining region, and XX males are genetically indistinguishable from XX females. The large NRRs show limited degeneration, with no evidence of gene loss, Y-linked copy decay, faster-X evolution or enrichment of sex-biased genes, and only modest repeat accumulation. Surprisingly, the coexisting Y haplotypes are neither independent sex-determining systems nor successive stages of a single degeneration trajectory. Instead, they share an ancestral Dmrt1-linked region whose X-Y divergence dates to [~]3.47-5.70 Mya, while present-day Y copies of this region remain nearly identical and the large NRRs have accumulated private mutations independently. We thus propose that the Y chromosome undergoes cyclic dynamics of differentiation: extreme heterochiasmy promotes rapid large NRRs formation, sex-reversed XY females recurrently restore X-Y recombination, gene conversion and/or rare Y-Y recombination may homogenize Y copies at the Dmrt1-linked region, and renewed male transmission drives subsequent Y-specific differentiation. The findings provide a genome-wide resolution to a central paradox in sex chromosome evolution: how sex chromosomes can experience extensive recombination suppression yet remain homomorphic and only weakly degenerated. By showing that heterochiasmy and sex reversal uncouple the physical extent, age, and degeneration of sex-linked regions, our study reframes homomorphic sex chromosomes as dynamic, repeatedly regenerated systems shaped by alternating phases of recombination suppression, restored X-Y recombination and renewed Y differentiation. Significance statementWhy many vertebrate sex chromosomes remain homomorphic despite long-term recombination suppression remains unresolved. Using whole-genome population genomics, doubled-haploid YY genomes, and transcriptomics in the common frog, we show that multiple coexisting Y haplotypes in a single pond share an old Dmrt1-linked sex-determining region but carry younger, independently differentiated Y chromosomes. This genome-wide resolution reveals that extreme heterochiasmy, where recombination is largely restricted to chromosome ends in males, can rapidly generate very large nonrecombining regions, while sex-reversed XY females can restore X-Y recombination and reduce divergence outside the Dmrt1-linked region. These opposing processes generate cyclic dynamics of Y differentiation rather than a directional path towards degeneration. Our study provides a mechanistic explanation for the persistence of co-existing multiple Y haplotypes in one population, maintenance of homomorphic sex chromosomes, and a broadly relevant framework for sex chromosome evolution in lineages with heterochiasmy and sex reversal.

evolutionary biology↗

bioRxiv2025

Evidence for an ancient master sex determination gene in Hymenoptera

The vast majority of Hymenopterans determine sex by haplodiploidy, in which males and females develop from haploid unfertilized and diploid fertilized eggs, respectively. At the molecular level, the majority of Hymenoptera are thought to determine sex by so-called Complementary Sex Determination (CSD). Under CSD, sex is determined by the feminizing effects of one or more allele-rich loci, in which the feminizing function is imparted by the interactions of functionally distinct alleles. Because of high allelic diversity, most diploids are heterozygous and develop as females, whereas haploid individuals develop as males, as do rare homozygous diploids. Despite diverse empirical results suggesting that CSD is widespread in Hymenopterans, and substantial theoretical and empirical study of the consequences of CSD, the molecular biology of CSD has received little attention outside of the honeybee, Apis mellifera. Available evidence provides support for divergent perspectives ranging from a single (nearly) universally-conserved CSD locus or a pattern dominated by evolutionary turnover with different genes serving as the CSD gene(s) in different lineages. Recently, a novel non-coding RNA gene named ANTSR was shown to serve as a CSD gene in different ant lineages, and the authors suggested that ANTSR might serve as a more broadly-conserved CSD gene. To assess the role of ANTSR role in CSD across diverse Hymenoptera, we studied syntenic conservation and polymorphism patterns in the broad ANTSR locus, genome-wide sequence from available male and female diploid Formica ants, and data from a sibling cross for Bombus terrestris. We find evidence that ANTSR is a conserved CSD gene across diverse Aculeata, the largest group of Hymenoptera, and provide preliminary evidence that Formica may have multiple CSD loci including ANTSR.

genetics↗

bioRxiv2025

Multiple origins of a sex ratio supergene in Formica ants

Many known supergenes, regions of the genome containing two or more functional mutations with little or no recombination between them, formed in recent evolutionary time to control complex traits. However, when supergenes persist through millions of years of evolution, they may take on additional functions in different lineages. Here, we investigate how an ancient supergene has evolved to gain novel function. In Formica ants, most species have an ancient "social" supergene with M and P haplotypes which determine whether a colony is headed by a single queen or multiple queens, respectively. At least three Formica species have an additional haplotype on the same chromosome, termed MD, associated with female-biased offspring sex ratio at the colony level. Is an MD haplotype present in additional species? Do the MD haplotypes share a common origin or did they evolve convergently? With whole-genome resequencing, we identify MD haplotypes in three additional species and use variation across six Formica species to examine the evolutionary history of the MD haplotype. We find that the MD haplotype did not originate from a rearrangement of the ancestral M haplotype. Instead, the MD haplotype likely originated from recombination between the M and P haplotypes. Strikingly, we identified two putative origins of the MD haplotype, one in the ancestor of five Nearctic species, and a second in the Palearctic species F. cinerea. The discovery of two MD haplotypes convergently evolving from distinct recombination events between two ancestral supergene haplotypes illustrates how supergenes can diversify and gain additional phenotypes.

genomics↗

bioRxiv2025

Variation in social organization and supergene control along a latitudinal gradient

Widespread species often experience vastly different environmental conditions across their range. In species with polymorphic traits under strong genetic control, we can investigate how environmental variation influences the distribution of traits and whether the strength of genetic control is consistent across environmental gradients. Here, we investigate the distribution of phenotypic and genetic variation in the ant Formica podzolica across 30{degrees} of latitude. This species shares a supergene that is associated with colony queen number and colony sex ratio with other congeners, but we detect a surprising six common supergene variants. Colonies with a single queen are more abundant in the north compared to those with multiple queens, although the queen number polymorphism is present throughout the range. In parallel, the frequency of supergene haplotypes also varies with latitude. Of the 170 colonies examined, 10.6% contained supergene haplotypes that did not match the queen number phenotype. The highest concentration of these mismatched colonies occurred in one site, raising the possibility that the environmental conditions there override supergene function. While the supergene system in F. podzolica is complex, this species holds promise for understanding how an ancient supergene system evolves in a single species experiencing highly variable environmental conditions.

evolutionary biology↗

bioRxiv2024

Migration strategies of a high-latitude breeding songbird (Setophaga coronata coronata) revealed using multi-sensor geolocators and stable isotopes

Seasonal migration allows animals to use habitat where conditions are unfavorable for part of the year but may constrain breeding ranges due to the costs of longer migrations as ranges expand poleward. In species with large ranges, high latitude breeding populations may employ different migratory strategies allowing them to persist far from other core non-breeding areas. The myrtle warbler (Setophaga coronata coronata) has two disjunct non-breeding ranges in North and Central America-one along the Gulf Coast and the other on the Pacific. Previous work indirectly linked birds breeding in Alaska with the Pacific non-breeding area, suggesting that high latitude populations evolved a shorter migration route. We directly tested this hypothesis using geolocators measuring both light and atmospheric pressure to track Alaskan myrtle warbler migration in fine detail and inferred non-breeding areas using hydrogen isotopes for a larger sample of birds breeding in Alaska, British Columbia, and Alberta. We found, contrary to expectations, that all geolocator-tracked birds and most birds with stable isotope data migrated to the southeastern United States, while only a small subset of birds ([~]5%) likely wintered on the Pacific Coast. We additionally demonstrate the advantages of pressure geolocation for characterizing migratory behavior at a fine scale.

animal behavior and cognition↗

bioRxiv2024

Unexpected absence of a multiple-queen supergene haplotype from supercolonial populations of Formica ants

Ants exhibit many complex social organization strategies. One particularly elaborate strategy is supercoloniality, in which a colony consists of many interconnected nests (=polydomy) with many queens (=polygyny). In many species of Formica ants, an ancient queen number supergene determines whether a colony is monogyne (=headed by single queen) or polygyne. The presence of the rearranged P haplotype typically leads colonies to be polygyne. However, the presence and function of this supergene polymorphism have not been examined in supercolonial populations. Here, we use genomic data from species in the Formica rufa group to determine whether the P haplotype leads to supercoloniality. In a Formica paralugubris population, we find that nests are polygyne, despite the absence of the P haplotype in workers. We find spatial genetic ancestry patterns in nests consistent with supercolonial organization. Additionally, we find that the P haplotype is also absent in workers from supercolonial Formica aquilonia, and Formica aquilonia x polyctena hybrid populations, but is present in some Formica polyctena workers. We conclude that the P haplotype is not necessary for supercoloniality in the Formica rufa group, despite its longstanding association with non-supercolonial polygyny across the Formica genus.

evolutionary biology↗

bioRxiv2024

Introgression across narrow contact zones shapes the genomic landscape of phylogenetic variation in an African bird clade

Genomic analyses of hybrid zones provide excellent opportunities to investigate the consequences of introgression in nature. In combination with phylogenomics analyses, hybrid zone studies may illuminate the role of ancient and contemporary gene flow in shaping variation of phylogenetic signals across the genome, but this avenue has not been explored yet. We combined phylogenomic and geographic cline analyses in a Pogoniulus tinkerbird clade to determine whether contemporary introgression through hybrid zones contributes to gene-tree heterogeneity across the species ranges. We found diverse phylogenetic signals across the genome with the most common topologies supporting monophyly among taxa connected by secondary contact zones. Remarkably, these systematic conflicts were also recovered when selecting only individuals from each taxons core range. Using analyses of derived allele sharing and "recombination aware" phylogenomics, we found that introgression shapes gene-tree heterogeneity, and the species tree most likely supports monophyletic red-fronted tinkerbirds, as recovered in previous reconstructions based on mitochondrial DNA. Furthermore, by fitting geographic clines across two secondary contact zones, we found that introgression rates were lower in genomic regions supporting the putative species tree compared to those supporting the two taxa in contact as monophyletic. This demonstrates that introgression through narrow contact zones shapes gene-tree heterogeneity even in allopatric populations. Finally, we did not find evidence that mitochondria-interacting nuclear genes acted as barrier loci. Our results show that species can withstand important amounts of introgression while maintaining their phenotypic integrity and ecological separation, raising questions regarding the genomic architecture of adaptation and barriers to gene flow.

evolutionary biology↗

bioRxiv2023

Does social antagonism facilitate supergene expansion? A novel region of suppressed recombination in a 4-haplotype supergene system.

Models of both sex chromosome evolution and the genetic basis of local adaptation suggest that selection acts to lock beneficial combinations of alleles together in regions of reduced or suppressed recombination. Drawing inspiration from such models, we apply similar logic to investigate whether an autosomal supergene underlying colony social organization in ants expanded to include "socially antagonistic" alleles. We tested this premise in a Formica ant species wherein we identified four supergene haplotypes on chromosome 3 underlying colony social organization and sex ratio. Remarkably, we discovered a novel rearranged supergene variant (9r) on chromosome 9 underlying queen miniaturization. The 9r is tightly linked to one of the haplotypes (P2) on chromosome 3, found predominantly in multi-queen (polygyne) colonies. We suggest that queen miniaturization is strongly disfavored in the single queen (monogyne) background, and thus socially antagonistic. As such, divergent selection experienced by ants living in alternative social environments (monogyne and polygyne) may have contributed to the emergence of a genetic polymorphism on chromosome 9 and associated queen size dimorphism. Consequently, an ancestral polygyne-associated haplotype may have expanded to include the polymorphism on chromosome 9, resulting in a larger region of suppressed recombination spanning two chromosomes. This process is analogous to the formation of neo-sex chromosomes and consistent with models of expanding regions of suppressed recombination. We also propose that miniaturized queens, 16-20% smaller than queens without 9r, could be incipient intraspecific social parasites. Significance statementWhen sets of gene variants work well together, selection may lead to a reduction in recombination between them. Here, we discover a novel supergene region on chromosome 9 that controls a previously undescribed queen size polymorphism in Formica cinerea ants. The haplotype that is found in small queens, 9r, is tightly linked to a supergene haplotype on chromosome 3 that is found in multi-queen colonies. We propose that the region of suppressed recombination expanded to include both chromosome 3 and chromosome 9 because small queens could be successful in the multi-queen but not in the single-queen environment.

evolutionary biology↗

bioRxiv2021

Comparing divergence landscapes from reduced-representation and whole-genome re-sequencing in the yellow-rumped warbler (Setophaga coronata) species complex

Researchers seeking to generate genomic data for non-model organisms are faced with a number of trade-offs when deciding which method to use. The selection of reduced representation approaches versus whole genome re-sequencing will ultimately affect the marker density, sequencing depth, and the number of individuals that can multiplexed. These factors can affect researchers ability to accurately characterize certain genomic features, such as landscapes of divergence--how FST varies across the genomes. To provide insight into the effect of sequencing method on the estimation of divergence landscapes, we applied an identical bioinformatic pipeline to three generations of sequencing data (GBS, ddRAD, and WGS) produced for the same system, the yellow-rumped warbler species complex. We compare divergence landscapes generated using each method for the myrtle warbler (Setophaga coronata coronata) and the Audubons warbler (S. c. auduboni), and for Audubons warblers with deeply divergent mtDNA resulting from mitochondrial introgression. We found that most high-FST peaks were not detected in the ddRAD dataset, and that while both GBS and WGS were able to identify the presence of large peaks, WGS was superior at a finer scale. Comparing Audubons warblers with divergent mitochondrial haplotypes, only WGS allowed us to identify small (10-20kb) regions of elevated differentiation, one of which contained the nuclear-encoded mitochondrial gene NDUFAF3. We calculated the cost per base pair for each method and found it was comparable between GBS and WGS, but significantly higher for ddRAD. These comparisons highlight the advantages of WGS over reduced representation methods when characterizing landscapes of divergence.

evolutionary biology↗

bioRxiv2021

Linked supergenes underlie split sex ratio and social organization in an ant

Sexually reproducing organisms usually invest equally in male and female offspring. Deviations from this pattern have led researchers to new discoveries in the study of parent-offspring conflict, genomic conflict, and cooperation. Some social insect species exhibit the unusual population-level pattern of split sex ratio, wherein some colonies specialize in the production of future queens and others specialize in the production of males. Theoretical work focused on the relatedness asymmetries emerging from haplodiploid inheritance, whereby queens are equally related to daughters and sons, but their daughter workers are more closely related to sisters than to brothers, led to a series of testable predictions and spawned many empirical studies of this phenomenon. However, not all empirical systems follow predicted patterns, so questions remain about how split sex ratio emerges. Here, we sequence the genomes of 138 Formica glacialis workers from 34 male-producing and 34 gyne-producing colonies to determine whether split sex ratio is under genetic control. We identify a supergene spanning 5.5 Mbp that is closely associated with sex allocation in this system. Strikingly, this supergene is adjacent to another supergene spanning 5 Mbp that is associated with variation in colony queen number. We identify a similar pattern in a second related species, Formica podzolica. The discovery that split sex ratio is determined, at least in part, by a supergene in two species opens a new line of research on the evolutionary drivers of split sex ratio. Significance StatementSome social insects exhibit split sex ratio, wherein some colonies produce future queens and others produce males. This phenomenon spawned many influential theoretical studies and empirical tests, both of which have advanced our understanding of parent-offspring conflicts and cooperation. However, some empirical systems did not follow theoretical predictions, indicating that researchers lack a comprehensive understanding of the drivers of split sex ratio. Here, we show that split sex ratio is associated with a large genomic region in two ant species. The discovery of a genetic basis for sex allocation in ants provides a novel explanation for this phenomenon, particularly in systems where empirical observations deviate from theoretical predictions.

evolutionary biology↗