Supergene degeneration opposes polymorphism: The curious case of balanced lethals

Supergenes offer some of the most spectacular examples of long-term balancing selection in nature but their origin and maintenance remain a mystery. A critical aspect of supergenes is reduced recombination between arrangements. Reduced recombination protects adaptive multi-trait phenotypes, but can also lead to degeneration through mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One such outcome is the formation of balanced lethal systems, a maladaptive system where both supergene arrangements have accumulated deleterious mutations to the extent that both homozygotes are inviable, leaving only heterozygotes to reproduce. Here, we perform a simulation study to understand the conditions under which these different outcomes occur, assuming a scenario of introgression after allopatric divergence. We found that AOD aids the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism is easily destabilized by further mutation accumulation. While degradation may strengthen AOD, thereby stabilizing the supergene polymorphism, it is often asymmetric, which is the key disrupter of the quasi-equilibrium state of the polymorphism. Furthermore, mechanisms that accelerate degeneration also tend to amplify asymmetric mutation accumulation between the supergene arrangements and vice versa. As the evolution of a balanced lethal system requires symmetric degradation of both arrangements, this leaves highly restricted conditions under which such a system could evolve. We show that small population size and low dominance coefficients are critical factors, as these reduce the efficacy of selection. The dichotomy between the persistence of a polymorphism and degradation of supergene arrangements likely underlies the rarity of balanced lethal systems in nature.

Ecogeography of Plumage Pigmentation In Great Horned Owls

ABSTRACT Plumage pigmentation is fundamental to a bird's phenotype, with pigment deposition causing relative crypsis or conspicuousness, depending on the environmental context. Geographic variation in plumage melanin tends to be predictable, suggesting that aspects of climate cause local matching of plumage to environment via genetic adaptation. Ecogeographic rules describe this predictability: Gloger's rule predicts that populations in wetter and warmer environments will be more pigmented; Bogert's Rule predicts more pigmentation in cold environments. The Great Horned Owl (Bubo virginianus) exhibits extensive geographic variation in the degree of melanin-based pigmentation. We examined fine-scale spatial variation in owl plumage melanism along environmental gradients in southwestern North America. We tested whether variation is explained by either of two non-mutually exclusive hypotheses: (1) a history of allopatric divergence between subspecies or (2) in situ local adaptation consistent with ecogeographic rules. The allopatric divergence hypothesis predicts a bimodal distribution of plumage melanism, with a geographic cline across a zone of secondary contact, whereas the local adaptation hypothesis predicts that climate explains variation independently of geography. Using a colorimeter, we measured coloration in 101 museum specimens of breeding-season Great Horned Owls that had been obtained from variable environments and elevations. Specimens previously identified as separate subspecies were distinguishable by colorimetry. Plumage lightness, however, was continuously distributed, rather than bimodal. While accounting for males having reduced pigmentation relative to females, linear models revealed that lighter plumage was associated with low latitude, low elevation, high temperature, and low precipitation. These findings suggest that variation in Great Horned Owl plumage pigmentation is best understood as continuous ecogeographic variation, consistent with ecogeographic predictions, and currently maintained in situ along multiple environmental gradients that characterize the “sky island” topography of the southwestern USA.

An introgression breakthrough left by an anthropogenic contact between two ascidians

Human-driven translocations of species have diverse evolutionary consequences such as promoting hybridization between previously geographically isolated taxa. This is well-illustrated by the solitary tunicate, Ciona robusta, native to the North East Pacific and introduced in the North East Atlantic. It is now co-occurring with its congener C. intestinalis in the English Channel, and C. roulei in the Mediterranean Sea. Despite their long allopatric divergence, first and second generation crosses showed a high hybridization success between the introduced and native taxa in the laboratory. However, previous genetic studies failed to provide evidence of recent hybridization between C. robusta and C. intestinalis in the wild. Using SNPs obtained from ddRAD-sequencing of 397 individuals from 26 populations, we further explored the genome-wide population structure of the native Ciona taxa. We first confirmed results documented in previous studies, notably i) a chaotic genetic structure at regional scale, and ii) a high genetic similarity between C. roulei and C. intestinalis, which is calling for further taxonomic investigation. More importantly, and unexpectedly, we also observed a genomic hotspot of long introgressed C. robusta tracts into C. intestinalis genomes at several locations of their contact zone. Both the genomic architecture of introgression, restricted to a 1.5 Mb region of chromosome 5, and its absence in allopatric populations suggest introgression is recent and occurred after the introduction of the non-indigenous species. Overall, our study shows that anthropogenic hybridization can be effective in promoting introgression breakthroughs between species at a late stage of the speciation continuum.

Genomic signatures of rapid adaptive divergence in a tropical montane species

Mountain regions contain extraordinary biodiversity. The environmental heterogeneity and glacial cycles often accelerate speciation and adaptation of montane species, but how these processes influence the genomic differentiation of these species is largely unknown. Using a novel chromosome-level genome and population genomic comparisons, we study allopatric divergence and selection in an iconic bird living in a tropical mountain region in New Guinea, Archbold's bowerbird ( Amblyornis papuensis ). Our results show that the two populations inhabiting the eastern and western Central Range became isolated ca 11 800 years ago, probably because the suitable habitats for this cold-tolerating bird decreased when the climate got warmer. Our genomic scans detect that genes in highly divergent genomic regions are over-represented in developmental processes, which is probably associated with the observed differences in body size between the populations. Overall, our results suggest that environmental differences between the eastern and western Central Range probably drive adaptive divergence between them.

Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)

Background Elucidating the effects of geography and selection on genetic variation is critical for understanding the relative importance of adaptation in driving differentiation and identifying the environmental factors underlying its occurrence. Adaptive genetic variation is common in tree species, especially widely distributed long-lived species. Pseudotaxus chienii can occupy diverse habitats with environmental heterogeneity and thus provides an ideal material for investigating the process of population adaptive evolution. Here, we characterize genetic and expression variation patterns and investigate adaptive genetic variation in P. chienii populations. Results We generated population transcriptome data and identified 13,545 single nucleotide polymorphisms (SNPs) in 5037 unigenes across 108 individuals from 10 populations. We observed lower nucleotide diversity (π = 0.000701) among the 10 populations than observed in other gymnosperms. Significant negative correlations between expression diversity and nucleotide diversity in eight populations suggest that when the species adapts to the surrounding environment, gene expression and nucleotide diversity have a reciprocal relationship. Genetic structure analyses indicated that each distribution region contains a distinct genetic group, with high genetic differentiation among them due to geographical isolation and local adaptation. We used FST outlier, redundancy analysis, and latent factor mixed model methods to detect molecular signatures of local adaptation. We identified 244 associations between 164 outlier SNPs and 17 environmental variables. The mean temperature of the coldest quarter, soil Fe and Cu contents, precipitation of the driest month, and altitude were identified as the most important determinants of adaptive genetic variation. Most candidate unigenes with outlier signatures were related to abiotic and biotic stress responses, and the monoterpenoid biosynthesis and ubiquitin-mediated proteolysis KEGG pathways were significantly enriched in certain populations and deserve further attention in other long-lived trees. Conclusions Despite the strong population structure in P. chienii, genomic data revealed signatures of divergent selection associated with environmental variables. Our research provides SNPs, candidate unigenes, and biological pathways related to environmental variables to facilitate elucidation of the genetic variation in P. chienii in relation to environmental adaptation. Our study provides a promising tool for population genomic analyses and insights into the molecular basis of local adaptation.

Comparative phylogeography of the freshwater mussels of the southeastern United States: reconstructing historic drainages using molecular data

Knowledge of species ages and their distribution enhance our understanding of processes that create and maintain species diversity at both local and regional levels. The largest family of freshwater mussels (Unionidae), reach their highest species diversity in drainages of the southeastern united states. By sequencing multiple loci from mussel species distributed throughout the drainages in this region, we attempt to uncover historical patterns of divergence and determine the role of vicariance events on the species formation in mussels and extend our hypothesis to freshwater animals in general. We analyzed 346 sequences from five genera encompassing 37 species. Species were sampled across 12 distinct drainages ending either in the Atlantic Ocean or the Gulf of Mexico. Overall the topologies of the different genera returned phylogenetic trees that were congruent with geographically contiguous drainages. The most common pattern was the grouping between the Atlantic slope and gulf coast drainages, however the Tennessee drainage was often the exception to this pattern grouping with the Atlantic slope. Most mussel species find a most recent common ancestor within a drainage before finding an ancestor between drainages. This supports the hypothesis of allopatric divergence followed by later burst of speciation within a drainage. Our estimated divergence times for the Atlantic-Gulf split agree with other studies estimating vicariance in fish species of the Atlantic and gulf coast.

Continental-scale gene flow prevents allopatric divergence of pelagic freshwater bacteria

Allopatric divergence is one of the principal mechanisms for speciation of macro-organisms. Microbes by comparison are assumed to disperse more freely and to be less limited by dispersal barriers. However, thermophilic prokaryotes restricted to geothermal springs have shown clear signals of geographic isolation, but robust studies on this topic for microbes with less strict habitat requirements are scarce. Furthermore, it has only recently been recognized that homologous recombination among conspecific individuals provides species coherence in a wide range of prokaryotes. Recombination barriers thus may define prokaryotic species boundaries, yet, the extent to which geographic distance between populations gives rise to such barriers is an open question. Here, we investigated gene flow and population structure in a widespread species of pelagic freshwater bacteria, Polynucleobacter paneuropaeus. Through comparative genomics of 113 conspecific strains isolated from freshwater lakes and ponds located across a North-South range of more than 3000 km, we were able to reconstruct past gene flow events. The species turned out to be highly recombinogenic as indicated by significant signs of gene transfer and extensive genome mosaicism. While genomic differences increased with spatial distance on a regional scale (< 170 km), such correlations were mostly absent on larger scales up to 3400 km. We conclude that allopatric divergence in European P. paneuropaeus is minor, and that effective gene flow across the sampled geographic range in combination with a high recombination efficacy maintains species coherence.

Topology Testing and Demographic Modeling Illuminate a Novel Speciation Pathway in the Greater Caribbean Sea Following the Formation of the Isthmus of Panama

Recent genomic analyses have highlighted the prevalence of speciation with gene flow in many taxa and have underscored the importance of accounting for these reticulate evolutionary processes when constructing species trees and generating parameter estimates. This is especially important for deepening our understanding of speciation in the sea where fast moving ocean currents, expanses of deep water, and periodic episodes of sea level rise and fall act as soft and temporary allopatric barriers that facilitate both divergence and secondary contact. Under these conditions, gene flow is not expected to cease completely while contemporary distributions are expected to differ from historical ones. Here we conduct range-wide sampling for Pederson’s cleaner shrimp (Ancylomenes pedersoni), a species complex from the Greater Caribbean that contains three clearly delimited mitochondrial lineages with both allopatric and sympatric distributions. Using mtDNA barcodes and a genomic ddRADseq approach, we combine classic phylogenetic analyses with extensive topology testing and demographic modeling (10 site frequency replicates x 45 evolutionary models x 50 model simulations/replicate = 22,500 simulations) to test species boundaries and reconstruct the evolutionary history of what was expected to be a simple case study. Instead, our results indicate a history of allopatric divergence, secondary contact, introgression, and endemic hybrid speciation driven by the final closure of the Isthmus of Panama and the strengthening of the Gulf Stream Current ~3.5 million years ago. The history of this species complex recovered by model-based methods that allow reticulation differs from that recovered by standard phylogenetic analyses and is unexpected given contemporary distributions. The geologically and biologically meaningful insights gained by our model selection analyses illuminate a novel pathway of species formation that resulted from one of the most biogeographically significant events in Earth’s history.