Biology subjects

Scarparo, G.

Publications and source records attributed to Scarparo, G..

4 recordsLinked to original sources

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↗

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↗

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↗