Individual-based Modeling of Genome Evolution in Haplodiploid Organisms.

Ants, bees, wasps, bark beetles, and other species have haploid males and diploid females. Although such haplodiploid species play key ecological roles and are threatened by environmental changes, no general framework exists for simulating their genetic evolution. Here, we use the SLiM simulation environment to build a novel model for individual-based forward simulation of genetic evolution in haplodiploids. We compare the fates of adaptive and deleterious mutations and find that selection on recessive mutations is more effective in haplodiploids than in diploids. Our open-source model will foster an understanding of the evolution of sociality and how ecologically important haplodiploid species may respond to changing environments.

Recurring adaptive introgression of a supergene variant that determines social organization.

Introgression has been proposed as an essential source of adaptive genetic variation. However, a key barrier to adaptive introgression is that recombination can break down combinations of alleles that underpin many traits. This barrier might be overcome in supergene regions, where suppressed recombination leads to joint inheritance across many loci. Here, we study the evolution of a large supergene region that determines a major social and ecological trait in Solenopsis fire ants: whether colonies have one queen or multiple queens. Using coalescent-based phylogenies built from the genomes of 365 haploid fire ant males, we show that the supergene variant responsible for multiple-queen colonies evolved in one species and repeatedly spread to other species through introgressive hybridization. This finding highlights how supergene architecture can enable a complex adaptive phenotype to recurrently permeate species boundaries.

Divergent genes in gerbils: prevalence, relation to GC-biased substitution, and phenotypic relevance.

BACKGROUND: Two gerbil species, sand rat (Psammomys obesus) and Mongolian jird (Meriones unguiculatus), can become obese and show signs of metabolic dysregulation when maintained on standard laboratory diets. The genetic basis of this phenotype is unknown. Recently, genome sequencing has uncovered very unusual regions of high guanine and cytosine (GC) content scattered across the sand rat genome, most likely generated by extreme and localized biased gene conversion. A key pancreatic transcription factor PDX1 is encoded by a gene in the most extreme GC-rich region, is remarkably divergent and exhibits altered biochemical properties. Here, we ask if gerbils have proteins in addition to PDX1 that are aberrantly divergent in amino acid sequence, whether they have also become divergent due to GC-biased nucleotide changes, and whether these proteins could plausibly be connected to metabolic dysfunction exhibited by gerbils. RESULTS: We analyzed ~ 10,000 proteins with 1-to-1 orthologues in human and rodents and identified 50 proteins that accumulated unusually high levels of amino acid change in the sand rat and 41 in Mongolian jird. We show that more than half of the aberrantly divergent proteins are associated with GC biased nucleotide change and many are in previously defined high GC regions. We highlight four aberrantly divergent gerbil proteins, PDX1, INSR, MEDAG and SPP1, that may plausibly be associated with dietary metabolism. CONCLUSIONS: We show that through the course of gerbil evolution, many aberrantly divergent proteins have accumulated in the gerbil lineage, and GC-biased nucleotide substitution rather than positive selection is the likely cause of extreme divergence in more than half of these. Some proteins carry putatively deleterious changes that could be associated with metabolic and physiological phenotypes observed in some gerbil species. We propose that these animals provide a useful model to study the 'tug-of-war' between natural selection and the excessive accumulation of deleterious substitutions mutations through biased gene conversion.

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants.

Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young 'social' supergene of fire ants, a powerful system for disentangling the effects of evolutionary antagonism and suppressed recombination. We hypothesize that gene degeneration and social antagonism shaped the evolution of the fire ant supergene, resulting in distinct patterns of gene expression. We test these ideas by identifying allelic differences between supergene variants, characterizing allelic expression across populations, castes and body parts, and contrasting allelic expression biases with differences in expression between social forms. We find strong signatures of gene degeneration and gene-specific dosage compensation. On this background, a small portion of the genes has the signature of adaptive responses to evolutionary antagonism between social forms.

Red fire ants (Solenopsis invicta) are native to South America, but the species has spread to North America, Australia and New Zealand where it can be an invasive pest. A reason for this species' invasiveness types of colonies : one with a single egg-laying queen and another with several queens. However, it is not possible to simply add more queens to a colony with one queen. Instead, the number of queens in a colony is controlled genetically, by a chromosome known as the 'social chromosome'. Like many other animals, red fire ants are diploid: their cells have two copies of each chromosome, which can carry two different versions of each gene. The social chromosome is no different, and it comes in two variants, SB and Sb. Each ant can therefore have either two SB chromosomes, leading to a colony with a single queen; or one SB chromosome and one Sb chromosome, leading to a colony with multiple queens. Ants with two copies of the Sb variant die when they are young, so the Sb version is inherited in a similar way to how the Y chromosome is passed on in humans. However, the social chromosome in red fire ants appeared less than one million years ago, making it much younger than the human Y chromosome, which is 180 million years old. This makes the social chromosome a good candidate for examining the early evolution of special chromosome variants that are only inherited. How differences between the SB and the Sb chromosomes are evolving is an open question, however. Perhaps each version of the social chromosome has been optimised through natural selection to one colony type. Another suggestion is that the Sb chromosome has degenerated over time because its genes cannot be 'reshuffled' as they would be on normal chromosomes. Martinez-Ruiz et al. compared genetic variants on the SB and Sb chromosomes, along with their expression in different types of ant colonies. The analysis showed that the Sb variant is in fact breaking down because of the lack of gene shuffling. This loss is compensated by intact copies of the same genes found on the SB variant, which explains why ants with the Sb variant can only survive if they also carry the SB version. Only a handful of genes on the social chromosomes appear to have been optimised by natural selection. Therefore Martinez-Ruiz et al. concluded the differences between the two chromosomes that lead to different colony types are collateral effects of Sb's inability to reshuffle its genes. This work reveals how a special chromosome similar to the Y chromosome in humans evolved. It also shows how multiple complex evolutionary forces can shape a species' genetic makeup and social forms.

Runaway GC Evolution in Gerbil Genomes.

Recombination increases the local GC-content in genomic regions through GC-biased gene conversion (gBGC). The recent discovery of a large genomic region with extreme GC-content in the fat sand rat Psammomys obesus provides a model to study the effects of gBGC on chromosome evolution. Here, we compare the GC-content and GC-to-AT substitution patterns across protein-coding genes of four gerbil species and two murine rodents (mouse and rat). We find that the known high-GC region is present in all the gerbils, and is characterized by high substitution rates for all mutational categories (AT-to-GC, GC-to-AT, and GC-conservative) both at synonymous and nonsynonymous sites. A higher AT-to-GC than GC-to-AT rate is consistent with the high GC-content. Additionally, we find more than 300 genes outside the known region with outlying values of AT-to-GC synonymous substitution rates in gerbils. Of these, over 30% are organized into at least 17 large clusters observable at the megabase-scale. The unusual GC-skewed substitution pattern suggests the evolution of genomic regions with very high recombination rates in the gerbil lineage, which can lead to a runaway increase in GC-content. Our results imply that rapid evolution of GC-content is possible in mammals, with gerbil species providing a powerful model to study the mechanisms of gBGC.

Degenerative Expansion of a Young Supergene.

Long-term suppression of recombination ultimately leads to gene loss, as demonstrated by the depauperate Y and W chromosomes of long-established pairs of XY and ZW chromosomes. The young social supergene of the Solenopsis invicta red fire ant provides a powerful system to examine the effects of suppressed recombination over a shorter timescale. The two variants of this supergene are carried by a pair of heteromorphic chromosomes, referred to as the social B and social b (SB and Sb) chromosomes. The Sb variant of this supergene changes colony social organization and has an inheritance pattern similar to a Y or W chromosome because it is unable to recombine. We used high-resolution optical mapping, k-mer distribution analysis, and quantification of repetitive elements on haploid ants carrying alternate variants of this young supergene region. We find that instead of shrinking, the Sb variant of the supergene has increased in length by more than 30%. Surprisingly, only a portion of this length increase is due to consistent increases in the frequency of particular classes of repetitive elements. Instead, haplotypes of this supergene variant differ dramatically in the amounts of other repetitive elements, indicating that the accumulation of repetitive elements is a heterogeneous and dynamic process. This is the first comprehensive demonstration of degenerative expansion in an animal and shows that it occurs through nonlinear processes during the early evolution of a region of suppressed recombination.

The fire ant social chromosome supergene variant Sb shows low diversity but high divergence from SB.

Variation in social behaviour is common, yet little is known about the genetic architectures underpinning its evolution. A rare exception is in the fire ant Solenopsis invicta: Alternative variants of a supergene region determine whether a colony will have exactly one or up to dozens of queens. The two variants of this region are carried by a pair of 'social chromosomes', SB and Sb, which resemble a pair of sex chromosomes. Recombination is suppressed between the two chromosomes in the supergene region. While the X-like SB can recombine with itself in SB/SB queens, recombination is effectively absent in the Y-like Sb because Sb/Sb queens die before reproducing. Here, we analyse whole-genome sequences of eight haploid SB males and eight haploid Sb males. We find extensive SB-Sb differentiation throughout the >19-Mb-long supergene region. We find no evidence of 'evolutionary strata' with different levels of divergence comparable to those reported in several sex chromosomes. A high proportion of substitutions between the SB and Sb haplotypes are nonsynonymous, suggesting inefficacy of purifying selection in Sb sequences, similar to that for Y-linked sequences in XY systems. Finally, we show that the Sb haplotype of the supergene region has 635-fold less nucleotide diversity than the rest of the genome. We discuss how this reduction could be due to a recent selective sweep affecting Sb specifically or associated with a population bottleneck during the invasion of North America by the sampled population.

Fire ant social chromosomes: Differences in number, sequence and expression of odorant binding proteins.

Variation in social behavior is common yet our knowledge of the mechanisms underpinning its evolution is limited. The fire ant Solenopsis invicta provides a textbook example of a Mendelian element controlling social organization: alternate alleles of a genetic element first identified as encoding an odorant binding protein (OBP) named Gp-9 determine whether a colony accepts one or multiple queens. The potential roles of such a protein in perceiving olfactory cues and evidence of positive selection on its amino acid sequence made it an appealing candidate gene. However, we recently showed that recombination is suppressed between Gp-9 and hundreds of other genes as part of a >19 Mb supergene-like region carried by a pair of social chromosomes. This finding raises the need to reassess the potential role of Gp-9. We identify 23 OBPs in the fire ant genome assembly, including nine located in the region of suppressed recombination with Gp-9. For six of these, the alleles carried by the two variants of the supergene-like region differ in protein-coding sequence and thus likely in function, with Gp-9 showing the strongest evidence of positive selection. We identify an additional OBP specific to the Sb variant of the region. Finally, we find that 14 OBPs are differentially expressed between single- and multiple-queen colonies. These results are consistent with multiple OBPs playing a role in determining social structure.

The genomic and phenotypic diversity of Schizosaccharomyces pombe.

Natural variation within species reveals aspects of genome evolution and function. The fission yeast Schizosaccharomyces pombe is an important model for eukaryotic biology, but researchers typically use one standard laboratory strain. To extend the usefulness of this model, we surveyed the genomic and phenotypic variation in 161 natural isolates. We sequenced the genomes of all strains, finding moderate genetic diversity (π = 3 × 10(-3) substitutions/site) and weak global population structure. We estimate that dispersal of S. pombe began during human antiquity (∼340 BCE), and ancestors of these strains reached the Americas at ∼1623 CE. We quantified 74 traits, finding substantial heritable phenotypic diversity. We conducted 223 genome-wide association studies, with 89 traits showing at least one association. The most significant variant for each trait explained 22% of the phenotypic variance on average, with indels having larger effects than SNPs. This analysis represents a rich resource to examine genotype-phenotype relationships in a tractable model.