Journal
MOLECULAR ECOLOGY
Volume 26, Issue 11, Pages 2864-2879Publisher
WILEY
DOI: 10.1111/mec.14054
Keywords
diversity in supergene variants; evolutionary strata; social chromosomes; Solenopsis invicta; queen number in ants
Funding
- Biotechnology and Biological Sciences Research Council [BB/K004204/1]
- Natural Environment Research Council [NE/L00626X/1]
- NERC EOS Cloud
- Queen Mary Innovation Ltd.
- QMUL Research-IT
- MidPlus computational facilities (Engineering and Physical Sciences Research Council) [EP/K000128/1]
- BBSRC [BB/K004204/1] Funding Source: UKRI
- EPSRC [EP/K000128/1] Funding Source: UKRI
- NERC [NE/L00626X/1] Funding Source: UKRI
- Biotechnology and Biological Sciences Research Council [BB/K004204/1] Funding Source: researchfish
- Engineering and Physical Sciences Research Council [EP/K000128/1] Funding Source: researchfish
- Natural Environment Research Council [NE/L00626X/1] Funding Source: researchfish
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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.
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