Publications by year
In Press
Paris JR, Whiting JR, Daniel MJ, Obiol JF, Parsons PJ, van der Zee MJ, Wheat CW, Hughes KA, Fraser BA (In Press). A large and diverse autosomal haplotype is associated with sex-linked colour polymorphism in the guppy.
Abstract:
A large and diverse autosomal haplotype is associated with sex-linked colour polymorphism in the guppy
ABSTRACTColour polymorphism provides a tractable trait that can be harnessed to explore the evolution of sexual selection and sexual conflict. Male colour patterns of the Trinidadian guppy (Poecilia reticulata) are governed by both natural and sexual selection, and are typified by extreme pattern colour variation as a result of negative frequency dependent selection. Since guppy colour patterns are often inherited faithfully from fathers to sons, it has been historically presumed that colour genes are physically linked to sex determining loci as a ‘supergene’ on the sex chromosome. Yet the actual identity and genomic location of the colour pattern genes has remained elusive. We phenotyped and genotyped four guppy ‘Iso-Y lines’, where colour was inherited along the patriline, but backcrossed into the stock population every 2 to 3 generations for 40 generations, thereby homogenising the genome at regions unrelated to colour. Using an unbiased phenotyping method to proportion colour pattern differences between and among the Iso-Y lines, we confirmed that the breeding design was successful in producing four distinct colour patterns. Our analysis of genome resequencing data of the four Iso-Y lines uncovered a surprising genetic architecture for colour pattern polymorphism. Genetic differentiation among Iso-Y lines was repeatedly associated with a large and diverse haplotype (∼5Mb) on an autosome (LG1), not the sex chromosome (LG12). Moreover, the LG1 haplotype showed elevated linkage disequilibrium and exhibited evidence of sex-specific diversity when we examined whole-genome sequencing data of the natural source population. We hypothesise that colour pattern polymorphism is driven by Y-autosome epistasis, and conclude that predictions of sexual conflict should focus on incorporating the effects of epistasis in understanding complex adaptive architectures.
Abstract.
Whiting JR, Paris JR, van der Zee MJ, Parsons PJ, Weigel D, Fraser BA (In Press). Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies.
Abstract:
Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies
ABSTRACTStudies of convergence in wild populations have been instrumental in understanding adaptation by providing strong evidence for natural selection. At the genetic level, we are beginning to appreciate that the re-use of the same genes in adaptation occurs through different mechanisms and can be constrained by underlying trait architectures and demographic characteristics of natural populations. Here, we explore these processes in naturally adapted high- (HP) and low-predation (LP) populations of the Trinidadian guppy, Poecilia reticulata. As a model for phenotypic change this system provided some of the earliest evidence of rapid and repeatable evolution in vertebrates; the genetic basis of which has yet to be studied at the whole-genome level. We collected whole-genome sequencing data from ten populations (176 individuals) representing five independent HP-LP river pairs across the three main drainages in Northern Trinidad. We evaluate population structure, uncovering several LP bottlenecks and variable between-river introgression that can lead to constraints on the sharing of adaptive variation between populations. Consequently, we found limited selection on common genes or loci across all drainages. Using a pathway type analysis, however, we find evidence of repeated selection on different genes involved in cadherin signalling. Finally, we found a large repeatedly selected haplotype on chromosome 20 in three rivers from the same drainage. Taken together, despite limited sharing of adaptive variation among rivers, we found evidence of convergent evolution associated with HP-LP environments in pathways across divergent drainages and at a previously unreported candidate haplotype within a drainage.
Abstract.
Whiting JR, Paris JR, Parsons PJ, Matthews S, Reynoso Y, Hughes KA, Reznick D, Fraser BA (In Press). On the genetic architecture of rapidly adapting and convergent life history traits in guppies.
Abstract:
On the genetic architecture of rapidly adapting and convergent life history traits in guppies
ABSTRACTThe genetic basis of traits can shape and constrain how adaptation proceeds in nature; rapid adaptation can be facilitated by polygenic traits, whereas polygenic traits may restrict re-use of the same genes in adaptation (genetic convergence). The rapidly evolving life histories of guppies in response to predation risk provide an opportunity to test this proposition. Guppies adapted to high- (HP) and low-predation (LP) environments in northern Trinidad evolve rapidly and convergently among natural populations. This system has been studied extensively at the phenotypic level, but little is known about the underlying genetic architecture. Here, we use an F2 QTL design to examine the genetic basis of seven (five female, two male) guppy life history phenotypes. We use RAD-sequencing data (16,539 SNPs) from 370 male and 267 female F2 individuals. We perform linkage mapping, estimates of genome-wide and per-chromosome heritability (multi-locus associations), and QTL mapping (single-locus associations). Our results are consistent with architectures of many-loci of small effect for male age and size at maturity and female interbrood period. Male trait associations are clustered on specific chromosomes, but female interbrood period exhibits a weak genome-wide signal suggesting a potentially highly polygenic component. Offspring weight and female size at maturity are also associated with a single significant QTL each. These results suggest rapid phenotypic evolution of guppies may be facilitated by polygenic trait architectures, but these may restrict gene-reuse across populations, in agreement with an absence of strong signatures of genetic convergence from recent population genomic analyses of wild HP-LP guppies.
Abstract.
2021
Whiting JR, Paris JR, van der Zee MJ, Parsons PJ, Weigel D, Fraser BA (2021). Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies.
PLOS Genetics,
17(5), e1009566-e1009566.
Abstract:
Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies
Studies of convergence in wild populations have been instrumental in understanding adaptation by providing strong evidence for natural selection. At the genetic level, we are beginning to appreciate that the re-use of the same genes in adaptation occurs through different mechanisms and can be constrained by underlying trait architectures and demographic characteristics of natural populations. Here, we explore these processes in naturally adapted high- (HP) and low-predation (LP) populations of the Trinidadian guppy, Poecilia reticulata. As a model for phenotypic change this system provided some of the earliest evidence of rapid and repeatable evolution in vertebrates; the genetic basis of which has yet to be studied at the whole-genome level. We collected whole-genome sequencing data from ten populations (176 individuals) representing five independent HP-LP river pairs across the three main drainages in Northern Trinidad. We evaluate population structure, uncovering several LP bottlenecks and variable between-river introgression that can lead to constraints on the sharing of adaptive variation between populations. Consequently, we found limited selection on common genes or loci across all drainages. Using a pathway type analysis, however, we find evidence of repeated selection on different genes involved in cadherin signaling. Finally, we found a large repeatedly selected haplotype on chromosome 20 in three rivers from the same drainage. Taken together, despite limited sharing of adaptive variation among rivers, we found evidence of convergent evolution associated with HP-LP environments in pathways across divergent drainages and at a previously unreported candidate haplotype within a drainage.
Abstract.
2020
Lange A, Paris JR, Gharbi K, Cézard T, Miyagawa S, Iguchi T, Studholme DJ, Tyler CR (2020). A newly developed genetic sex marker and its application to understanding chemically induced feminisation in roach (. Rutilus rutilus. ).
Molecular Ecology Resources,
20(4), 1007-1022.
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Fraser BA, Whiting JR, Paris JR, Weadick CJ, Parsons PJ, Charlesworth D, Bergero R, Bemm F, Hoffmann M, Kottler VA, et al (2020). Improved Reference Genome Uncovers Novel Sex-Linked Regions in the Guppy (Poecilia reticulata).
Genome Biology and Evolution,
12(10), 1789-1805.
Abstract:
Improved Reference Genome Uncovers Novel Sex-Linked Regions in the Guppy (Poecilia reticulata)
Abstract
. Theory predicts that the sexes can achieve greater fitness if loci with sexually antagonistic polymorphisms become linked to the sex determining loci, and this can favor the spread of reduced recombination around sex determining regions. Given that sex-linked regions are frequently repetitive and highly heterozygous, few complete Y chromosome assemblies are available to test these ideas. The guppy system (Poecilia reticulata) has long been invoked as an example of sex chromosome formation resulting from sexual conflict. Early genetics studies revealed that male color patterning genes are mostly but not entirely Y-linked, and that X-linkage may be most common in low-predation populations. More recent population genomic studies of guppies have reached varying conclusions about the size and placement of the Y-linked region. However, this previous work used a reference genome assembled from short-read sequences from a female guppy. Here, we present a new guppy reference genome assembly from a male, using long-read PacBio single-molecule real-time sequencing and chromosome contact information. Our new assembly sequences across repeat- and GC-rich regions and thus closes gaps and corrects mis-assemblies found in the short-read female-derived guppy genome. Using this improved reference genome, we then employed broad population sampling to detect sex differences across the genome. We identified two small regions that showed consistent male-specific signals. Moreover, our results help reconcile the contradictory conclusions put forth by past population genomic studies of the guppy sex chromosome. Our results are consistent with a small Y-specific region and rare recombination in male guppies.
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Sherman KD, Paris J, King RA, Moore KA, Dahlgren CP, Knowles LC, Stump K, Tyler CR, Stevens JR (2020). RAD-Seq Analysis and in situ Monitoring of Nassau Grouper Reveal Fine-Scale Population Structure and Origins of Aggregating Fish.
FRONTIERS IN MARINE SCIENCE,
7 Author URL.
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2019
Paris JR, Usher J (2019). Functional genomic characterization of metallothioneins in brown trout (Salmo trutta L.). using synthetic genetic analysis.
Scientific Reports,
9(1).
Abstract:
Functional genomic characterization of metallothioneins in brown trout (Salmo trutta L.). using synthetic genetic analysis
Metal pollution has made a significant impact on the earth’s ecosystems and tolerance to metals in a wide variety of species has evolved. Metallothioneins, a group of cysteine-rich metal-ion binding proteins, are known to be a key physiological mechanism in regulating protection against metal toxicity. Many rivers across the southwest of England are detrimentally affected by metal pollution, but brown trout (Salmo trutta L.) populations are known to reside within them. In this body of work, two isoforms of metallothionein (MetA and MetB) isolated from trout occupying a polluted and a control river are examined. Using synthetic genetic array (SGA) analyses in the model yeast, Saccharomyces cerevisiae, functional genomics is used to explore the role of metallothionein isoforms in driving metal tolerance. By harnessing this experimental system, S. cerevisiae is used to (i) determine the genetic interaction maps of MetA and MetB isoforms; (ii) identify differences between the genetic interactions in both isoforms and (iii) demonstrate that pre-exposure to metals in metal-tolerant trout influences these interactions. By using a functional genomics approach leveraged from the model yeast Saccharomyces cerevisiae, we demonstrate how such approaches could be used in understanding the ecology and evolution of a non-model species.
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Paris JR, Usher J (2019). Publisher Correction: Functional genomic characterization of metallothioneins in brown trout (Salmo trutta L.). using synthetic genetic analysis.
Sci Rep,
9(1).
Abstract:
Publisher Correction: Functional genomic characterization of metallothioneins in brown trout (Salmo trutta L.). using synthetic genetic analysis.
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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2018
Ikediashi C, Paris JR, King RA, Beaumont WRC, Ibbotson A, Stevens JR (2018). Atlantic salmon Salmo salar in the chalk streams of England are genetically unique.
J Fish Biol,
92(3), 621-641.
Abstract:
Atlantic salmon Salmo salar in the chalk streams of England are genetically unique.
Recent research has identified genetic groups of Atlantic salmon Salmo salar that show association with geological and environmental boundaries. This study focuses on one particular subgroup of the species inhabiting the chalk streams of southern England, U.K. These fish are genetically distinct from other British and European S. salar populations and have previously demonstrated markedly low admixture with populations in neighbouring regions. The genetic population structure of S. salar occupying five chalk streams was explored using 16 microsatellite loci. The analysis provides evidence of the genetic distinctiveness of chalk-stream S. salar in southern England, in comparison with populations from non-chalk regions elsewhere in western Europe. Little genetic differentiation exists between the chalk-stream populations and a pattern of isolation by distance was evident. Furthermore, evidence of temporal stability of S. salar populations across the five chalk streams was found. This work provides new insights into the temporal stability and lack of genetic population sub-structuring within a unique component of the species' range of S. salar.
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Paris JR, Sherman KD, Bell E, Boulenger C, Delord C, El-Mahdi MBM, Fairfield EA, Griffiths AM, Gutmann Roberts C, Hedger RD, et al (2018). Understanding and managing fish populations: keeping the toolbox fit for purpose.
J Fish Biol,
92(3), 727-751.
Abstract:
Understanding and managing fish populations: keeping the toolbox fit for purpose.
Wild fish populations are currently experiencing unprecedented pressures, which are projected to intensify in the coming decades. Developing a thorough understanding of the influences of both biotic and abiotic factors on fish populations is a salient issue in contemporary fish conservation and management. During the 50th Anniversary Symposium of the Fisheries Society of the British Isles at the University of Exeter, UK, in July 2017, scientists from diverse research backgrounds gathered to discuss key topics under the broad umbrella of 'Understanding Fish Populations'. Below, the output of one such discussion group is detailed, focusing on tools used to investigate natural fish populations. Five main groups of approaches were identified: tagging and telemetry; molecular tools; survey tools; statistical and modelling tools; tissue analyses. The appraisal covered current challenges and potential solutions for each of these topics. In addition, three key themes were identified as applicable across all tool-based applications. These included data management, public engagement, and fisheries policy and governance. The continued innovation of tools and capacity to integrate interdisciplinary approaches into the future assessment and management of fish populations is highlighted as an important focus for the next 50 years of fisheries research.
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2017
Paris JR, Stevens JR, Catchen JM (2017). Lost in parameter space: a road map for. stacks.
Methods in Ecology and Evolution,
8(10), 1360-1373.
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2015
Paris JR, King RA, Stevens JR (2015). Human mining activity across the ages determines the genetic structure of modern brown trout (Salmo trutta L.) populations.
Evolutionary ApplicationsAbstract:
Human mining activity across the ages determines the genetic structure of modern brown trout (Salmo trutta L.) populations
Humans have exploited the earth's metal resources for thousands of years leaving behind a legacy of toxic metal contamination and poor water quality. The southwest of England provides a well-defined example, with a rich history of metal mining dating to the Bronze Age. Mine water washout continues to negatively impact water quality across the region where brown trout (Salmo trutta L.) populations exist in both metal-impacted and relatively clean rivers. We used microsatellites to assess the genetic impact of mining practices on trout populations in this region. Our analyses demonstrated that metal-impacted trout populations have low genetic diversity and have experienced severe population declines. Metal-river trout populations are genetically distinct from clean-river populations, and also from one another, despite being geographically proximate. Using approximate Bayesian computation (ABC), we dated the origins of these genetic patterns to periods of intensive mining activity. The historical split of contemporary metal-impacted populations from clean-river fish dated to the Medieval period. Moreover, we observed two distinct genetic populations of trout within a single catchment and dated their divergence to the Industrial Revolution. Our investigation thus provides an evaluation of contemporary population genetics in showing how human-altered landscapes can change the genetic makeup of a species.
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