The Influence of Supergenes on the Evolutionary Process
Locking together beneficial traits, supergenes confer significant evolutionary advantages. However, this association comes with potential costs, as it becomes exceedingly challenging to eliminate detrimental mutations.
Traditionally, it has been believed that sexual reproduction evolved as a means for organisms to mix or recombine different alleles (gene variations) in the next generation, creating essential genetic variation for natural selection and adaptation. However, recent research indicates that not all genome regions undergo equal shuffling. Some regions, containing a few to hundreds of genes, rarely undergo recombination.
Consequently, the same combination of alleles is consistently passed on together to the next generation, forming genetic units known as “supergenes.” These supergenes have been identified in various organisms such as ants, butterflies, birds, fish, plants, and fungi, with more likely awaiting discovery.
Scientists propose that supergenes evolve similarly to sex chromosomes. Over evolutionary time, alleles that benefit males but not females are selected to be transmitted together. This process leads to the development of regions with suppressed recombination, as seen between the X and Y chromosomes in mammals. This region can expand as more advantageous alleles for one sex but not the other accumulate near the initial region of suppressed recombination.
The Role of Supergenes in Regulating Traits and Social Organization
This phenomenon is known as sexually antagonistic selection. Recent findings reveal that sex chromosomes represent just a specific instance of a more extensive phenomenon. Supergenes, characterized by suppressed recombination, can play a role in regulating various traits, extending beyond sex chromosomes. Notably, they can influence social organization, as observed in the case of Formica wood ants.
“There exists an evolutionary force known as antagonistic selection, expected to drive the expansion of sex chromosomes, and the presence of this force was anticipated to manifest in supergenes as well. We are now confirming this phenomenon for the first time,” explains Buck Trible, an expert in ant supergenes at Harvard University.
Supergenes play a significant role in shaping the organization of Formica wood ant societies. These ants possess a supergene on chromosome 3 that determines whether colonies have a single or multiple queens. A recent discovery by researchers at the University of California, Riverside, unveiled another supergene on chromosome 9 in these wood ants. This supergene regulates the size of queens, with one variant producing miniature queens approximately 20 percent smaller than the standard-sized queens.
Association Between Miniature Queens and Multi-Queen Colonies
The study revealed that miniature queens are predominantly found in colonies with multiple queens. In essence, the version of the supergene on chromosome 9 associated with multi-queen colonies is closely linked to the version of the supergene on chromosome 3 responsible for generating miniature queens.
The chromosomes do not exhibit physical fusion, and the researchers noted that over 20 percent of ant eggs display “mismatched” supergene combinations. For example, an ant might possess the version of chromosome 3 responsible for single-queen colonies and, simultaneously, the version of chromosome 9 generating miniature queens. However, only a small proportion of individuals with these mismatches survive to adulthood, indicating robust selection against such combinations.
Entomologist Giulia Scarparo, the lead author of the study, explains, “Our hypothesis is that in cases of mismatches, individuals tend to develop into workers instead of queens.” Moreover, “there is a mechanism that negatively impacts the development of these individuals, explaining why we rarely observe this mismatch in the adult stage.”
The researchers term the strong selection against mismatched combinations “socially antagonistic” selection, as it parallels the sexually antagonistic selection that propels the evolution of sex chromosomes.
In single-queen colonies, mature queens typically embark on a nuptial flight to establish new colonies, utilizing body fat and muscles for the initial brood. Limited metabolic resources challenge small queens in independent colony establishment, leading to increased efficiency in thriving within multiple-queen colonies.
Evolutionary Role of Multi-Queen Colonies in the Emergence of Miniature Queens
The researchers propose that the evolution of multi-queen colonies was crucial for the emergence of miniature queens. These smaller queens rely on resources from workers produced by other queens in multi-queen colonies to support their offspring. Some miniature queens disproportionately invest resources in producing more of their kind, potentially displaying social parasitic behavior within the colony. Scarparo suggests, “The small queens may function as social parasites.”
Numerous workerless social-parasite ant species, totaling several hundred, exploit the resources of close relatives’ nests for their brood. The evolution of these socially parasitic species is still a mystery, but social supergenes likely play a role.
Suppression of recombination in supergenes often involves chromosomal inversions, flipping a section and reversing the gene sequence order. This hinders alignment and recombination during meiosis, the cell division process generating sex cells. The absence of genetic shuffling can permanently link two beneficial mutations in different genes. Marcus Kronforst, a researcher of supergenes in butterflies at the University of Chicago, explains, “Once an inversion occurs, the genetic variation accompanying the beneficial mutations is essentially forever locked with them, resembling a historical accident.”
Understanding the Dynamics of Genes in Supergenes
In many supergenes, including the social supergene in these ants, numerous genes collaborate, while others are bystanders in the region of suppressed recombination. The wood ants’ social supergene comprises about 500 genes, with only a small fraction directly contributing to the colony queen number, notes Jessica Purcell, the senior author of the study and an ant researcher at UC Riverside.
This arrangement not only influences the evolution of traits directly controlled by supergenes but also impacts all traits regulated by genes within the supergene. While beneficial combinations are locked together, regions of suppressed recombination may accumulate harmful mutations, posing challenges for their removal due to their association with other advantageous traits in the supergene.
Maintaining multiple supergene versions in the population involves a trade-off, as explained by Kronforst: “You’ll have some benefit associated with the inversion haplotype, but there’s also some detriment associated with it because it’s forever connected with some amount of deleterious genetic variation.”
Unveiling the Role of a Supergene in Swallowtail Butterflies
Kronforst investigates a supergene in swallowtail butterflies that regulates both the color pattern and shape of their wings. In Papilio polytes, females can display four distinct wing color patterns, with three mimicking different poisonous butterflies. To comprehend this supergene, Kronforst’s team sequenced the swallowtail genome, anticipating hundreds of genes. Unexpectedly, they found that a lone gene, doublesex, controls both wing shape and color. This gene, originally involved in governing sexual dimorphism within a species, has been adapted by butterflies to regulate wing patterning specifically in females.
In the swallowtail butterfly, doublesex exhibits four versions (haplotypes) within an inverted supergene, preventing recombination within the gene. This is essential to preserve distinct wing patterns, preventing a blend that would expose butterflies to predators. Kronforst’s team explores mimicry regulation in Papilio polytes relatives, discovering other species using doublesex without inversions to separate haplotypes. The absence of recombination prevention mechanisms in these species raises questions about how butterflies avoid blending wing patterns, highlighting inversions as just one means to suppress recombination.
Purcell underscores that comprehending recombination variation across the genome is a frontier in evolutionary thinking, influencing the trajectory of traits’ evolution.
Read the orihinal article on: SCIAM
Read more: Crocodile’s ‘Virgin Birth’ is a First for Science’s History Books
