A narrow window for geographic cline analysis using genomic data: Effects of age, drift, and migration on error rates

Jofre, Gaston I.; Rosenthal, Gil G.

doi:10.1111/1755-0998.13428

Cited by 12 publications

(7 citation statements)

References 73 publications

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“…Similarly, neutral clines generated by secondary contact can take a long time to decay, making them hard to distinguish from selected ones (Barton & Hewitt, 1985; Endler, 1977). Localized drift (and sampling effects) tends to distort cline shapes in a way that may lead to the discovery of false positives (Jofre & Rosenthal, 2021; Polechova & Barton, 2011). In addition, even though a genomic region may contain a large‐effect barrier locus, it might not show a cline if the genomic window is too broad to capture the relevant signatures.…”

Section: Discussionmentioning

confidence: 99%

Integrating top‐down and bottom‐up approaches to understand the genetic architecture of speciation across a monkeyflower hybrid zone

et al. 2023

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Understanding the phenotypic and genetic architecture of reproductive isolation is a long‐standing goal of speciation research. In several systems, large‐effect loci contributing to barrier phenotypes have been characterized, but such causal connections are rarely known for more complex genetic architectures. In this study, we combine “top‐down” and “bottom‐up” approaches with demographic modelling toward an integrated understanding of speciation across a monkeyflower hybrid zone. Previous work suggests that pollinator visitation acts as a primary barrier to gene flow between two divergent red‐ and yellow‐flowered ecotypes of Mimulus aurantiacus. Several candidate isolating traits and anonymous single nucleotide polymorphism loci under divergent selection have been identified, but their genomic positions remain unknown. Here, we report findings from demographic analyses that indicate this hybrid zone formed by secondary contact, but that subsequent gene flow was restricted by widespread barrier loci across the genome. Using a novel, geographic cline‐based genome scan, we demonstrate that candidate barrier loci are broadly distributed across the genome, rather than mapping to one or a few “islands of speciation.” Quantitative trait locus (QTL) mapping reveals that most floral traits are highly polygenic, with little evidence that QTL colocalize, indicating that most traits are genetically independent. Finally, we find little evidence that QTL and candidate barrier loci overlap, suggesting that some loci contribute to other forms of reproductive isolation. Our findings highlight the challenges of understanding the genetic architecture of reproductive isolation and reveal that barriers to gene flow other than pollinator isolation may play an important role in this system.

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Section: Discussionmentioning

confidence: 99%

Integrating top‐down and bottom‐up approaches to understand the genetic architecture of speciation across a monkeyflower hybrid zone

et al. 2023

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“…It is reasonable to hypothesize that loci with c shifted to north are good candidates for harbouring genes with P. carbonelli alleles under positive selection that confer advantage in the genomic background or habitat of P. bocagei . Note, however, that genetic drift in hybrid zones can increase false positives when testing for adaptive introgression (Jofre & Rosenthal, 2021) and affect clines shape (Polechová & Barton, 2011). Drift is higher in smaller demes with lower migration rates among demes.…”

Section: Discussionmentioning

confidence: 99%

Hybridization in late stages of speciation: Strong but incomplete genome‐wide reproductive isolation and ‘large Z‐effect’ in a moving hybrid zone

et al. 2023

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In organisms reproducing sexually, speciation occurs when increasing divergence results in pre-or post-zygotic reproductive isolation between lineages. Studies focusing on reproductive isolation origin in early stages of speciation are common and many rely on genomic scans to infer introgression providing limited information on the genomic architecture of reproductive isolation long-term maintenance. This study analyses a natural hybrid zone between two species in a late stage of speciation. We used ddRADseq genotyping in the contact between Podarcis bocagei and P. carbonelli to examine admixture extent, analyse hybrid zone stability and assess genome-wide variation in selection against introgression. We confirmed strong but incomplete reproductive isolation in a bimodal hybrid zone. New findings revealed population genetic structure within P. carbonelli in the contact zone; geographical and genomic clines analysis suggested strong selection against gene flow, but a relatively small proportion of the loci can introgress, mostly within the narrow contact zone. However, geographical clines revealed that a few introgressed loci show signs of potential positive selection, particularly into P. bocagei. Geographical clines also detected a signal of hybrid zone movement towards P. bocagei distribution. Genomic cline analysis revealed heterogeneous patterns of introgression among loci within the syntopy zone, but the majority maintain a strong association with the genomic background of origin. However, incongruences between both cline approaches were found, potentially driven by confounding effects on genomic clines. Last, an important role of the Z chromosome in reproductive isolation is suggested. Importantly, overall patterns of restricted introgression seem to result from numerous strong intrinsic barriers across the genome.

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“…Strong physical or environmentally mediated barriers to dispersal may affect model performance (Ringbauer et al 2018, Wang & Bradburd 2014, Bradburd et al 2013). In a similar vein, our model ignores confounding factors such as local adaptation that may drive clinal patterns of relatedness (e.g., Pruisscher et al 2018; Jofre & Rosenthal 2021).…”

Section: Discussionmentioning

confidence: 99%

A spatial approach to jointly estimate Wright’s neighborhood size and long-term effective population size

Hancock

Toczydlowski

Bradburd

2023

Preprint

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Spatially continuous patterns of genetic differentiation, which are common in nature, are often poorly described by existing population genetic theory or methods that assume panmixia or discrete, clearly definable populations. There is therefore a need for statistical approaches in population genetics that can accommodate continuous geographic structure, and that ideally use georeferenced individuals as the unit of analysis, rather than populations or subpopulations. In addition, researchers are often interested describing the diversity of a population distributed continuously in space, and this diversity is intimately linked to the dispersal potential of the organism. A statistical model that leverages information from patterns of isolation-by-distance to jointly infer parameters that control local demography (such as Wright's neighborhood size), and the long-term effective size (Ne) of a population would be useful. Here, we introduce such a model that uses individual-level pairwise genetic and geographic distances to infer Wright's neighborhood size and long-term Ne. We demonstrate the utility of our model by applying it to complex, forward-time demographic simulations as well as an empirical dataset of the Red Sea clownfish (Amphiprion bicinctus). The model performed well on simulated data relative to alternative approaches and produced reasonable empirical results given the natural history of clownfish. The resulting inferences provide important insights into the population genetic dynamics of spatially structure populations.

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A narrow window for geographic cline analysis using genomic data: Effects of age, drift, and migration on error rates

Cited by 12 publications

References 73 publications

Integrating top‐down and bottom‐up approaches to understand the genetic architecture of speciation across a monkeyflower hybrid zone

Integrating top‐down and bottom‐up approaches to understand the genetic architecture of speciation across a monkeyflower hybrid zone

Hybridization in late stages of speciation: Strong but incomplete genome‐wide reproductive isolation and ‘large Z‐effect’ in a moving hybrid zone

A spatial approach to jointly estimate Wright’s neighborhood size and long-term effective population size

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