- Butterfly Genetics Group, University of Cambridge, Cambridge, United Kingdom
- Adaptation, Evo-Devo, Evolutionary Ecology, Genome Evolution, Genotype-Phenotype, Hybridization / Introgression, Phylogenetics / Phylogenomics, Population Genetics / Genomics, Speciation
Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow in a butterfly
Is genetic diversity enhanced by a supergene?Recommended by Chris Jiggins based on reviews by Christelle Fraïsse and 2 anonymous reviewers
The butterfly species Heliconius numata has a remarkable wing pattern polymorphism, with multiple pattern morphs all controlled by a single genetic locus, which harbours multiple inversions. Each morph is a near-perfect mimic of a species in the fairly distantly related genus of butterflies, Melinaea.
The article by Rodríguez de Cara et al (2023) argues that the balanced polymorphism at this single wing patterning locus actually has a major effect on genetic diversity across the whole genome. First, polymorphic populations within H. numata are more dioverse than those without polymorphism. Second, H. numata is more genetically diverse than other related species and finally reconstruction of historical demography suggests that there has been a recent increase in effective population size, putatively associated with the acquisition of the supergene polymorphism. The supergene itself generates disassortative mating, such that morphs prefer to mate with others dissimilar to themselves - in this way it is similar to mechanisms for preventing inbreeding such as self-incompatibility loci in plants. This provides a potential mechanism whereby non-random mating patterns could increase effective population size. The authors also explore this mechanism using forward simulations, and show that mating patterns at a single locus can influence linked genetic diversity over a large scale.
Overall, this is an intriguing study, which suggests a far more widespread genetic impact of a single locus than might be expected. There are interesting parallels with mechanisms of inbreeding prevention in plants, such as the Pin/Thrum polymorphism in Primula, which also rely on mating patterns determined by a single locus but presumably also influence genetic diversity genome-wide by promoting outbreeding.
Rodríguez de Cara MÁ, Jay P, Rougemont Q, Chouteau M, Whibley A, Huber B, Piron-Prunier F, Ramos RR, Freitas AVL, Salazar C, Silva-Brandão KL, Torres TT, Joron M (2023) Balancing selection at a wing pattern locus is associated with major shifts in genome-wide patterns of diversity and gene flow. bioRxiv, 2021.09.29.462348, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.09.29.462348
Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula
Strange reproductive modes and population geneticsRecommended by Chris Jiggins based on reviews by Arnaud Estoup, Simon Henry Martin and 2 anonymous reviewers
There are many organisms that are asexual or have unusual modes of reproduction. One such quasi-sexual reproductive mode is androgenesis, in which the offspring, after fertilization, inherits only the entire paternal nuclear genome. The maternal genome is ditched along the way. One group of organisms which shows this mode of reproduction are clams in the genus Corbicula, some of which are androecious, while others are dioecious and sexual. The study by Vastrade et al. (2022) describes population genetic patterns in these clams, using both nuclear and mitochondrial sequence markers.
In contrast to what might be expected for an asexual lineage, there is evidence for significant genetic mixing between populations. In addition, there is high heterozygosity and evidence for polyploidy in some lineages. Overall, the picture is complicated! However, what is clear is that there is far more genetic mixing than expected. One possible mechanism by which this could occur is 'nuclear capture' where there is a mixing of maternal and paternal lineages after fertilization. This can sometimes occur as a result of hybridization between 'species', leading to further mixing of divergent lineages. Thus the group is clearly far from an ancient asexual lineage - recombination and mixing occur with some regularity.
The study also analyzed recent invasive populations in Europe and America. These had reduced genetic diversity, but also showed complex patterns of allele sharing suggesting a complex origin of the invasive lineages.
In the future, it will be exciting to apply whole genome sequencing approaches to systems such as this. There are challenges in interpreting a handful of sequenced markers especially in a system with polyploidy and considerable complexity, and whole-genome sequencing could clarify some of the outstanding questions,
Overall, this paper highlights the complex genetic patterns that can result through unusual reproductive modes, which provides a challenge for the field of population genetics and for the recognition of species boundaries.
Vastrade M, Etoundi E, Bournonville T, Colinet M, Debortoli N, Hedtke SM, Nicolas E, Pigneur L-M, Virgo J, Flot J-F, Marescaux J, Doninck KV (2022) Substantial genetic mixing among sexual and androgenetic lineages within the clam genus Corbicula. bioRxiv, 590836, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/590836