Strong hybrid male incompatibilities impede the spread of a selfish chromosome between populations of a fly

Verspoor, Rudi L.; Smith, Jack; Mannion, Natasha L. M.; Hurst, Gregory D. D.; Price, Tom A. R.

doi:10.1101/248237

Cited by 7 publications

(12 citation statements)

References 34 publications

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“…Sympatric populations have been documented in a wide range of taxa from insects to large mammals, in both terrestrial and aquatic environments, as well as in plants (Attard et al, 2016; Guo et al, 2018; Knutsen et al, 2018; Orlov et al, 2012; Ravinet et al, 2016; Schönswetter et al, 2007; Verspoor et al, 2018). Theoretically, they can represent a continuum of genomic divergence dependent on their evolutionary history with respect to degree of isolation over time (Roux et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Whole‐genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes

et al. 2021

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Section: Introductionmentioning

confidence: 99%

Whole‐genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes

et al. 2021

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“…Sympatric populations have been documented in a wide range of taxa from insects to large mammals, in both terrestrial and aquatic environments, as well as in plants (Attard, Beheregaray, & Möller, 2016;Guo et al, 2018;Knutsen et al, 2018;Orlov et al, 2012;Ravinet et al, 2016;Schönswetter et al, 2007;Verspoor, Smith, Mannion, Hurst, & Price, 2018). Theoretically, they can represent a continuum of genomic divergence dependent on their evolutionary history with respect to degree of isolation over time (Roux et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Whole-genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes

Saha¹,

Andersson²,

Kurland³

et al. 2021

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The sympatric existence of genetically distinct populations of the same species remains a puzzle in ecology. Coexisting salmonid fish populations are known from over 100 freshwater lakes. Most studies of sympatric populations have used limited numbers of genetic markers making it unclear if genetic divergence involves only certain parts of the genome. We return to the first reported case of salmonid sympatry, initially detected through contrasting homozygosity at a single allozyme locus (lactate dehydrogenase, LDH-A1) in brown trout in the small Lakes Bunnersjöarna, central Sweden. We use DNA from samples collected in the 1970s and a 96 SNP fluidigm array to verify the existence of the coexisting demes. We then apply whole-genome resequencing of pooled DNA to explore genome-wide diversity within and between these demes; strong genetic divergence is observed with genome-wide FST=0.13. Nucleotide diversity is estimated to 0.0013 in Deme I but only 0.0005 in Deme II. Individual whole-genome resequencing of two individuals per deme suggests considerably higher inbreeding in Deme II vs. Deme I. Comparing with similar data from other lakes we find that the genome-wide divergence between the demes is similar to that between reproductively isolated populations. We located two genes for LDH-A and found divergence between the demes in a regulatory section of one of the genes, but we could not find a perfect fit between allozyme and sequence data. Our data demonstrate genome-wide divergence governed by genetic drift and diversifying selection, confirming reproductive isolation between the sympatric demes.

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“…Such driving X -chromosomes have been detected in multiple species of both Drosophilidae and Diopsidae, and are commonly associated with chromosomal rearrangements ( Gershenson 1928 ; Sturtevant and Dobzhansky 1936 ; Stalker 1961 ; Jungen 1967 ; de Carvalho et al 1989 ; James and Jaenike 1990 ; Jaenike 1996 , 2001 ; Presgraves et al 1997 ; Yang et al 2004 ; Tao et al 2007 ; Unckless et al 2015 ; Keais et al 2017 ). Unchecked, these selfish genetic elements are expected to fix in populations, leading to eventual population extinction ( Hamilton 1967 ; Wallace 1968 ; Lyttle 1977 ), yet SR chromosomes are often observed at stable frequencies and in some cases form long-term geographic clines ( Sturtevant and Dobzhansky 1936 ; Dobzhansky 1944 , p. 78; James and Jaenike 1990 ; Beckenbach 1996 ; Atlan et al 1997 ; Dyer 2012 ; Verspoor et al 2018 ). Furthermore, some SR chromosomes paradoxically have ancient origins but no suppressors, motivating interest in identifying the forces acting to maintain SR chromosomes across evolutionary timescales ( Price et al 2019 ).…”

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confidence: 99%

Extensive Recombination Suppression and Epistatic Selection Causes Chromosome-Wide Differentiation of a Selfish Sex Chromosome inDrosophila pseudoobscura

et al. 2020

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Sex-Ratio (SR) chromosomes are selfish X-chromosomes that distort Mendelian segregation and are commonly associated with inversions. These chromosomal rearrangements suppress recombination with Standard (ST) X-chromosomes and are hypothesized to maintain multiple alleles important for drive in a single large haplotype. Here, we conduct a multifaceted study of the multiply inverted Drosophila pseudoobscura SR chromosome to understand the evolutionary history, genetic architecture, and present-day dynamics that shape this enigmatic selfish chromosome. The D. pseudoobscura SRchromosome has three non-overlapping inversions: basal, medial, and terminal. We find that 23 of 29 Mb of the D. pseudoobscura XR chromosome arm is highly differentiated between the Standard (ST) and SR arrangements, including a 6.6Mb collinear region between the medial and terminal inversions. Although crossing-over is heavily suppressed on this chromosome arm, we discover it is not completely eliminated, with measured rates indicating recombination suppression alone cannot explain patterns of differentiation or the near-perfect association of the three SR chromosome inversions in nature. We then demonstrate the ancient basal and medial inversions of the SR chromosome contain genes sufficient to cause weak drive. In contrast, the younger terminal inversion cannot drive by itself, but contains at least one modifier gene necessary for full manifestation of strong sex chromosome drive. By parameterizing population genetic models for chromosome-wide linkage disequilibrium with our experimental results, we infer that strong selection acts to maintain the near-perfect association of SR chromosome inversions in present day populations. Based on comparative genomic analyses, direct recombination experiments, segregation distortion assays, and population genetic modelling, we conclude the combined action of suppressed recombination and strong, ongoing, epistatic selection shape the D. pseudoobscura SR arrangement into a highly differentiated chromosome.

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Strong hybrid male incompatibilities impede the spread of a selfish chromosome between populations of a fly

Cited by 7 publications

References 34 publications

Whole‐genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes

Whole‐genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes

Whole-genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes

Extensive Recombination Suppression and Epistatic Selection Causes Chromosome-Wide Differentiation of a Selfish Sex Chromosome inDrosophila pseudoobscura

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