Epistatic mutations under divergent selection govern phenotypic variation in the crow hybrid zone

Knief, Ulrich; Bossu, Christen M.; Saino, Nicola; Hansson, Bengt; Poelstra, Jelmer W.; Vijay, Nagarjun; Weissensteiner, Matthias H.; Wolf, Jochen B. W.

doi:10.1038/s41559-019-0847-9

Cited by 70 publications

(110 citation statements)

References 57 publications

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“…Chromosome 18 only represents 1.22% of the entire assembly, corresponding to añ 8.5-fold enrichment of highly differentiated SV. Given that outliers are located in the proximity of previously identified genes presumably under divergent selection (such as AXIN2 and RGS9, Supplementary Table 4), this supports a crucial role of chromosome 18 in maintaining plumage divergence 24,25 .…”

Section: Resultssupporting

confidence: 61%

“…(Supplementary Table 4). Ten of these outliers (10.31%) were placed on chromosome 18, which was previously identified by SNP-based analyses as a candidate genomic region subject to divergent selection between the taxa [23][24][25] . Chromosome 18 only represents 1.22% of the entire assembly, corresponding to añ 8.5-fold enrichment of highly differentiated SV.…”

Section: Resultsmentioning

confidence: 99%

“…Only few narrow genomic regions associated with morphological contrast are subject to divergent selection reducing local gene flow and increasing genetic differentiation 23,24 . In the European hybrid zone comprising carrion crows (C. (c.) corone) and hooded crows (C. (c.) cornix) epistasis between a genetic factor on chromosome 18 and the gene NDP located on chromsome 1 explained most of the morphological variation 25 , which can be near-exclusively related to gene expression differences in melanocytes of nascent feathers 26,27 . Despite some indication for a structural rearrangement underlying phenotypic divergence in two European crow populations 24 , the overall extent and role of SV in population divergence remains unclear in this system.…”

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confidence: 99%

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Discovery and population genomics of structural variation in a songbird genus

et al. 2020

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Structural variation (SV) constitutes an important type of genetic mutations providing the raw material for evolution. Here, we uncover the genome-wide spectrum of intra-and interspecific SV segregating in natural populations of seven songbird species in the genus Corvus. Combining short-read (N = 127) and long-read re-sequencing (N = 31), as well as optical mapping (N = 16), we apply both assembly-and read mapping approaches to detect SV and characterize a total of 220,452 insertions, deletions and inversions. We exploit sampling across wide phylogenetic timescales to validate SV genotypes and assess the contribution of SV to evolutionary processes in an avian model of incipient speciation. We reveal an evolutionary young (~530,000 years) cis-acting 2.25-kb LTR retrotransposon insertion reducing expression of the NDP gene with consequences for premating isolation. Our results attest to the wealth and evolutionary significance of SV segregating in natural populations and highlight the need for reliable SV genotyping.

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Section: Resultssupporting

confidence: 61%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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Discovery and population genomics of structural variation in a songbird genus

et al. 2020

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“…These systems allow genomic regions with relevant differences to stand out clearly against a background of relatively low genetic differentiation. Examples include Heliconius butterflies 15,16 , Anopheles mosquitos 17,18 , pea aphids 19 , stick insects 20 , sunflowers 21 , monkeyflowers 22 , house mice 23,24 , threespine stickleback 25 and cichlid 26 fish, and various birds, including carrion and hooded crows [27][28][29] , flycatchers 30 , and blue-and golden-winged warblers 31 . In addition to enabling investigation of the genetic architecture of reproductive barriers, these systems allow many other questions to be addressed, such as what is the timeline of speciation, and what are the roles of chromosomal rearrangements and sex chromosomes 1 ?…”

Section: Main Text Introductionmentioning

confidence: 99%

Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps

Hejase

Salman‐Minkov

Campagna

et al. 2020

Preprint

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Numerous studies of emerging species have identified genomic "islands" of elevated differentiation against a background of relative homogeneity. The causes of these islands remain unclear, however, with some signs pointing toward "speciation genes" that locally restrict gene flow and others suggesting selective sweeps that have occurred within nascent species after speciation. Here, we examine this question through the lens of recently obtained genome sequence data for five species of southern capuchino seedeaters, finch-like birds from South America that have undergone a species radiation during the last ~50,000 generations. By applying newly developed statistical methods for ancestral recombination graph inference and machine-learning methods for the prediction of selective sweeps, we show that the striking islands of differentiation in these birds appear to be generally associated with relatively recent, speciesspecific selective sweeps, most of which are predicted to be "soft" sweeps acting on standing genetic variation. Many of these sweeps coincide with genes associated with melanin-based variation in plumage, suggesting a prominent role for sexual selection. At the same time, a few loci also exhibit indications of possible selection against gene flow. These observations shed new light on the complex manner in which natural selection shapes genome sequences during speciation.

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“…Non-additive interactions among species-specific alleles have received great attention, especially regarding genetic incompatibilities damaging hybrid fitness 32 . In contrast, we still know little how non-additive interactions influence in the phenotypic distribution of hybrid populations 48 . Since non-additive interactions are largely not heritable 49 , increased phenotypic novelty or variability in F1 hybrids do not directly indicate enhanced evolvability of hybrid populations.…”

Section: Discussionmentioning

confidence: 99%

Non-additive genetic effects induce novel phenotypic distributions in male mating traits of F1 hybrids

Atsumi¹,

Lagisz²,

Nakagawa³

2020

Preprint

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Hybridization is a source of phenotypic novelty and variation because of increased additive genetic variation. Yet, the roles of non-additive allelic interactions in shaping phenotypic mean and variance of hybrids have been underappreciated. Here we examine the distributions of male-mating traits in F1 hybrids via a meta-analysis of 3208 effect sizes from 39 animal species pairs. Although additivity sets phenotypic distributions of F1s to be intermediate, F1s also showed dominance and maternal inheritance. F1s expressed novel phenotypes (beyond the range of both parents) in 65% of species pairs, often associated with increased phenotypic variability. Overall, however, F1s expressed smaller variation than parents in 51% of traits. While genetic divergence between parents did not impact phenotypic novelty, it increased phenotypic variability of F1s. By creating novel phenotypes with increased variability, non-additivity of heterozygotic genome may play key roles in determining mating success of F1s, and their subsequent extinction or speciation.

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Epistatic mutations under divergent selection govern phenotypic variation in the crow hybrid zone

Cited by 70 publications

References 57 publications

Discovery and population genomics of structural variation in a songbird genus

Discovery and population genomics of structural variation in a songbird genus

Genomic islands of differentiation in a rapid avian radiation have been driven by recent selective sweeps

Non-additive genetic effects induce novel phenotypic distributions in male mating traits of F1 hybrids

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