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Fraser, B. A.

Publications and source records attributed to Fraser, B. A..

10 recordsLinked to original sources

Temporal genomics reveals rapid parallel adaptation in experimental populations of Trinidadian guppies (Poecilia reticulata)

Understanding the genomic basis of early adaptation is a central question in evolutionary biology. Although there is ongoing debate about whether early adaptation is more likely to be driven by polygenic responses or by loci of large effect, few studies of natural populations have been able to address this problem. Furthermore, early adaptation to a novel environment often coincides with founding events, making it difficult to disentangle neutral effects from adaptive genomic changes. Here we take advantage of the unique in situ guppy experimental system, in which we established replicate populations by translocating guppies from a high predation locality to four low predation localities. We present whole genome sequencing from the source population and the four experimental populations, sampled after [~]8-10 generations (first period), and again at [~]18-22 generations (second period). We find signatures of inbreeding only in the first period, despite documented population crashes in the second period. We show genome-wide dynamics of selection as well as selective change at single loci and uncover new targets of selection. Overall, we found signatures of selection at all levels; genome-wide, chromosome, and individual windows are more repeatable among replicates in the first period than in the second period.

evolutionary biology↗

Evolutionary divergence and adaptive potential of scototaxis in juvenile Trinidadian Guppies

Habitat choice and resource acquisition represent an intrinsic trade-off, resulting in variation among individuals and potentially local adaptation among populations. Here, we quantify scototaxis, or preference for dark versus light backgrounds, in juvenile guppies. Scototaxis assays, in which individuals choose between safer dark and riskier light backgrounds, are widely used as a measure of boldness in small fishes, but they can equally be interpreted as choice between two habitats. By rearing and testing 586 fish descended from ten natural populations from Trinidad under common garden conditions, we first quantify (broad sense) heritable variation, i.e. evolutionary potential, within populations. Next, we test for evolutionary divergence among populations in mean preference, and if present, whether ancestral predation regime is a mediator of divergence. Finally, we ask whether families and/or populations differ in the amount of behavioural variation they contain. Preference varied among families (12% of total variance), consistent with broad-sense heritable variation. We also found that mean preference varied among populations (11% of total variance explained). Evolutionary divergence among-populations is partly explained by ancestral predation regime, with populations from low-predation sites showing a stronger preference for dark backgrounds than high-predation populations from the same river. Additionally, we find that within-population behavioural variation is greater in high-predation populations. We conclude that guppy populations contain heritable variation that could facilitate adaptive evolution if scototaxis is subject to natural selection. Furthermore, while genetic drift may also contribute to evolutionary divergence among-populations, observed patterns are qualitatively consistent with local adaption to predation regime. Our results suggests that high predation sites favour bolder habitat choice on average, but also that local predation regime shapes the evolutionary dynamics of variation, perhaps by maintaining shy-bold variation among individuals, or by favouring individuals with less-predictable behaviour.

evolutionary biology↗

Repeated signatures of balancing selection in small and large populations of guppies (Poecilia reticulata)

Balancing selection is a powerful evolutionary force that maintains adaptive genetic and phenotypic diversity. Although methods to detect the footprints of balancing selection in genomic data have advanced, we still lack a clear understanding of how repeatable these signatures appear in wild populations, and how this repeatability is shaped by demographic history and existing genetic variation. The Trinidadian guppy (Poecilia reticulata) provides an ideal model to test the repeatability of balancing selection in the wild as there is strong evidence that negative frequency-dependent selection (NFDS) maintains colour polymorphism. Analysing whole-genome sequencing data from 11 guppy populations (n = 195) with contrasting demographic contexts, we apply scans of balancing selection to explore which genomic regions show evidence of repeatability. We find that populations with small Ne show less genetic repeatability but still exhibit population-specific regions of elevated diversity, implicating independent balancing selection or other evolutionary mechanisms. Despite this, we identify 23 regions with repeated signatures of balancing selection, including a region on LG22 containing genes involved in colour, vision, mate choice, and social behaviour. Investigating the repeatability of balancing selection in small and large populations improves our knowledge of how demographic factors interact with selective processes to shape natural variation.

evolutionary biology↗

AF-vapeR: A multivariate genome scan for detecting parallel evolution using allele frequency change vectors

O_LIThe repeatability of evolution at the genetic level has been demonstrated to vary along a continuum from complete parallelism to divergence. In order to better understand why this continuum exists within and among systems, hypotheses must be tested using high confidence sets of candidate loci for repeatability. Despite this, few methods have been developed to scan SNP data for signatures specifically associated with repeatability, as opposed to local adaptation. C_LIO_LIHere we present AF-vapeR (Allele Frequency Vector Analysis of Parallel Evolutionary Responses), an approach designed to identify genome regions exhibiting highly correlated allele frequency changes within haplotypes and among replicated allele frequency change vectors. The method divides the genome into windows of an equivalent number of SNPs, and within each window performs eigen decomposition over normalised allele frequency change vectors (AFV), each derived from a replicated pair of populations/species. Properties of the resulting eigenvalue distribution can be used to compare regions of the genome for those exhibiting strong parallelism, and can also be compared against a null distribution derived from randomly permuted AFV. Further, the shape of the eigenvalue distribution can reveal multiple axes of parallelism within datasets. C_LIO_LIWe demonstrate the utility of this approach to detect different modes of parallel evolution using simulations, and also demonstrate a reduction in error rate compared with intersecting FST outliers. Lastly, we apply AF-vapeR to three previously published datasets (stickleback, guppies, and Galapagos finches) which comprise a range of sampling and sequencing strategies, and lineage ages. We detect known parallel regions whilst also identifying novel candidates. C_LIO_LIThe main benefits of this approach include a reduced false-negative rate under many conditions, an emphasis on signals associated specifically with repeatable evolution as opposed to local adaptation, and an opportunity to identify different modes of parallel evolution at the first instance. C_LI

evolutionary biology↗

A large and diverse autosomal haplotype is associated with sex-linked colour polymorphism in the guppy

Colour 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.

evolutionary biology↗

On the genetic architecture of rapidly adapting and convergent life history traits in guppies

The 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.

evolutionary biology↗

Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)

It is now accepted that phenotypic evolution can occur quickly but the genetic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity to study this phenomenon. Guppy populations that were transplanted from high-predation (HP) to low-predation (LP) environments have been shown to mimic naturally-colonised LP populations phenotypically in as few as 8 generations. The new phenotypes persist in subsequent generations in lab environments, indicating their high heritability. Here, we compared whole genome variation in four populations recently introduced into LP sites along with the corresponding HP source population. We examined genome-wide patterns of genetic variation to estimate past demography, and uncovered signatures of selection with a combination of genome scans and a novel multivariate approach based on allele frequency change vectors. We were able to identify a limited number of candidate loci for convergent evolution across the genome. In particular, we found a region on chromosome 15 under strong selection in three of the four populations, with our multivariate approach revealing subtle parallel changes in allele frequency in all four populations across this region. Investigating patterns of genome-wide selection in this uniquely replicated experiment offers remarkable insight into the mechanisms underlying rapid adaptation, providing a basis for comparison with other species and populations experiencing rapidly changing environments. IMPACT STATEMENTThe genetic basis of rapid adaptation to new environments is largely unknown. Here we take advantage of a unique replicated experiment in the wild, where guppies from a high predation source were introduced into four low predation localities. Previous reports document census size fluctuations and rapid phenotypic evolution in these populations. We used genome-wide sequencing to understand past demography and selection. We detected clear signals of population growth and bottlenecks at the genome-wide level matching known census population data changes. We then identified candidate regions of selection across the genome, some of which were shared between populations. In particular, using a novel multivariate method, we identified parallel allele frequency change at a strong candidate locus for adaptation to low predation. These results and methods will be of use to those studying evolution at a recent, ecological timescale.

evolutionary biology↗

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 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.

evolutionary biology↗

Improved reference genome uncovers novel sex-linked regions in the guppy (Poecilia reticulata)

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 favour 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 colour 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 (SMRT) 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.

evolutionary biology↗

Contingent Convergence: The ability to detect convergent genomic evolution is dependent on demographic similarity

Outlier scans, in which the genome is scanned for signatures of selection, have become a prominent tool in studies of local adaptation, and more recently studies of genetic convergence in natural populations. However, such methods have the potential to be confounded by features of demographic history, such as population size and migration, which are considerably varied across natural populations. In this study, we use forward-simulations to investigate and illustrate how several measures of genetic differentiation commonly used in outlier scans (FST, DXY and {Delta}{pi}) are influenced by demographic variation across multiple sampling generations. In a factorial design with 16 treatments, we manipulate the presence/absence of founding bottlenecks (N of founding individuals), protracted bottlenecks (proportional size of diverging population) and migration rate between two populations with ancestral and derived phenotypic optima. Our results illustrate known constraints of individual measures associated with reduced population size and a lack of migration; but notably we demonstrate how relationships between measures are similarly dependent on demography. We find that false-positive signals of convergent evolution (the same simulated outliers detected in independent treatments) are attainable as a product of similar demographic treatment, and that outliers across different measures (particularly FST and DXY) can occur with little influence of selection. Taken together, we show how underappreciated, yet quantifiable measures of demographic history can influence commonly employed methods for detecting selection.

evolutionary biology↗