Author contributions DCJ coordinated all analyses, isolated DNA for sequencing, analysed and filtered SNP calls, conducted diversity analysis and GWAS and drafted the manuscript. CR produced phenotype data for growth on various solid media and growth rates in liquid media. AR conducted analysis of dating using mitochondrial data. DS conducted GWAS. MP analysed all phenotype data. TM identified LTR transposon insertions and analysed transposon insertion data. FXM conducted crosses for analysis of spore viability ZI produced indel calls with Cortex. WL conducted analysis of recombination rate, linkage disequilibrium decay and PCA for distance between strains. TMKC assisted with phenotype and population analysis. RP analysed Cortex and GATK indel calls. MM conducted amino acid profiling. JLDL and AC produced automated measures of cell morphology. SB aligned reads and produced GATK SNP calls. GH analysed population structure using fineSTRUCTURE. BO'F estimated the TMRCA from the nuclear genome using ACG. TK identified LTR transposon insertions JTS produced de novo assemblies. LB developed the custom Workspace workflow Spotsizer. BT assisted with sequence analysis. DAB assisted with analysis of novel genes. TS assisted with strain verification. SC produced images of wild strains and assisted with strain verification. JEEUH assisted with SNP validation. LvT and MT assisted with LTR validation. LJ and JL assisted with manual measures of cell morphology and FACS. SA produced gene expression data. MF, KM and ND assisted with sequencing. WB initiated and assisted with strain collection. JH coordinated manual measures of cell morphology and FACS. RECS coordinated automated measures of cell morphology. MR coordinated amino acid profiling. NM conducted analysis of recombination, linkage disequilibrium and advised on aspects of diversity and GWAS. DJB advised on GWAS. RD facilitated sequencing. JB contributed to the initiation and development of the project and financed the JB laboratory. AccessionsSequence data are archived in the European Nucleotide Archive (www.ebi.ac.uk/ena/), Study Accessions PRJEB2733 and PRJEB6284 (Supplementary Table 7). All SNPs and indels were submitted to NCBI dbSNP (www.ncbi.nlm.nih.gov/SNP/). Accessions are 974514578-974688138 (SNPs) and 974702618-974688139 (indels). Europe PMC Funders Group AbstractNatural 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 utility of this model, we surveyed the genomic and phenotypic variation in 161 natural isolates. We sequenced the genomes of all strains, revealing moderate genetic diversity (π = 3 ×10 −3 ) and weak global population structure. We estimate that dispersal of S. pombe began within human antiquity (~340 BCE), and ancestors of these strains reached the Americas at ~1623 CE. We quantified 74 traits, revealing substantial heritable phenotypic diversity. We cond...

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.

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.

No abstract

Suppressed recombination ultimately leads to gene loss, as demonstrated by the depauperate Y chromosomes of long-established XY pairs. To understand the shorter term effects, we used high-resolution optical mapping and k-mer distribution analysis on a young non-recombining region of fire ant social chromosomes. Instead of shrinking, the region has increased in length by more than 30%. This demonstrates that degenerative expansion can occur during the early evolution of non-recombining regions.