Biology subjects

Lagunas-Robles, G.

Publications and source records attributed to Lagunas-Robles, G..

8 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

Hidden in the genomic bycatch: insights into genome reorganization and population structure of the parasitic nematode Contortylenchus reversus

Insect-parasitic nematodes are widespread and often significantly reduce host fitness, yet we know surprisingly little about most species. Contortylenchus reversus is a hemocoel-inhabiting parasitic nematode that infects Dendroctonus bark beetles, notably impacting host mobility and fecundity. We first detail a chromosome-scale genome assembly of C. reversus, recovered serendipitously from a sequencing project targeting a host (Dendroctonus ponderosae). We assembled the 79.4 Mb genome into nine linkage groups and, through transcriptome-aided annotation, identified 11,244 protein-coding genes. Synteny comparisons with the only relatives for which there are complete assemblies reveal extensive chromosomal rearrangements and extreme loss of gene collinearity suggesting these insect-parasitic nematodes may have exceptionally malleable genomes. Using this genome assembly and repurposed reduced-representation genomic data from 707 D. ponderosae individuals, we investigated infection frequencies and population structure, identifying infection rates ranging from 0% to 50% across 18 geographically widespread collection sites. Population structure of C. reversus appears broadly concordant with the structure of the host beetle, suggesting a shared evolutionary history, while genetic variation (nucleotide diversity) in the parasitic nematode is highly reduced in comparison to its host. These results offer insights into its population genetics, host associations, and the evolutionary dynamics of a nematode-beetle interaction and highlight how genomic bycatch can reveal previously hidden details about an important species in a complex community.

genomics↗

bioRxiv2026

The tortured past of young polymorphic sex chromosomes revealed through multiple de novo genome assemblies of the mountain pine beetle

Neo-sex chromosomes provide a powerful system for studying the early stages of sex chromosome evolution and the genomic mechanisms that may contribute to reproductive isolation. Using PacBio long-read HiFi sequencing, Hi-C scaffolding, and sex-specific transcriptomic data, we generated six chromosome-level assemblies (male and female from three populations) of the mountain pine beetle (Dendroctonus ponderosae), a species known to harbor three partially reproductively isolated neo-Y haplogroups. These assemblies reveal that the large neo-X and neo-Y chromosomes formed through sequential fusions of the ancestral X with three autosomes, with recombination cessation occurring at [~]8.6, [~]6.3, and [~]4.3 MYA for each event. Comparative analyses show that while neo-X chromosomes remain largely collinear across populations, neo-Ys exhibit dramatic structural divergence, with 900-1,200 inverted segments per haplogroup and only [~]65% of sequence able to be aligned to the neo-X. Repeat analyses demonstrate moderate TE accumulation on the neo-Y, particularly LTR elements, and gene mapping analyses reveal extensive degeneration: [~]62% of neo-Y genes exhibit gene loss, fragmentation, or disruptive mutations. All populations retain a single pseudoautosomal region (PAR), though PAR size and gene content vary due to neo-Y specific rearrangements. Across neo-Ys, 27 genes are uniquely missing in the Western haplogroup, including previously identified candidates implicated in hybrid male sterility. Broader comparisons among neo-Ys show widespread structural variation, population specific patterns of degeneration, and limited gene family expansions. Together, these results provide the first full characterization of neo-sex chromosome evolution in D. ponderosae, revealing rapid, lineage specific neo-Y degeneration and highlighting the potential for sex chromosome divergence to contribute to emerging reproductive incompatibilities within a single species.

genomics↗

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↗

bioRxiv2025

Evidence of parental care as a novel reproductive isolating mechanism

Variation in behavior can contribute to reproductive isolation by preventing gene flow among populations. Here, we tested the novel hypothesis that parental care, when dysregulated, can function as a reproductive isolating mechanism in three-spined stickleback fish (Gasterosteus aculeatus). In the typical "common" stickleback ecotype, males provide care to their offspring by fanning with their pectoral fins and defending their nest. In contrast, a divergent "white" stickleback ecotype has evolutionarily lost care and disperses embryos into the surrounding environment. We examined how paternal care from common, white, and F1 hybrid fathers influenced offspring survival. We detected no intrinsic incompatibilities in embryos, but F1 hybrid fathers exhibited dysregulated parental care that coincided with decreased survival of parented offspring. The increased offspring mortality may be explained by further dysregulation of feeding and parenting circuitry, as F2 hybrids exhibited significantly higher rates of post-fertilization filial cannibalism than common or white fathers. Additionally, despite strong divergence in nesting-building and courtship behavior, F1 hybrids achieved mating success at a similar rate as male commons and whites, suggesting that prezygotic barriers against hybrids may be weak. The observed postzygotic isolation, and potentially weak prezygotic isolation in lab-based studies, suggest that hybridization is likely occurring at low rates in the wild. Population genetic analysis supported this, as low proportions of putative hybrids were detected in sympatric sites. Together, these results may help explain why genetic divergence between these phenotypically distinct ecotypes is low and provide evidence that dysregulated parental behavior can act as a newly discovered postzygotic reproductive isolating barrier.

evolutionary biology↗

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↗

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↗