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

Abstract

Although rapid phenotypic evolution has been documented often, the genomic 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 evolve toward the phenotypes of naturally colonized LP populations in as few as eight generations. These changes persist in common garden experiments, indicating that they have a genetic basis. Here, we report results of whole genome variation in four experimental populations colonizing LP sites along with the corresponding HP source population. We examined genome‐wide patterns of genetic variation to estimate past demography and used a combination of genome scans, forward simulations, and a novel analysis of allele frequency change vectors to uncover the signature of selection. We detected clear signals of population growth and bottlenecks at the genome‐wide level that matched the known history of population numbers. We found a region on chromosome 15 under strong selection in three of the four populations and 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.

Genetic depletion does not prevent rapid evolution in island‐introduced lizards

“…Experimental evolution with controlled field manipulations can help alleviate the challenges via a priori knowledge of the original source population, the time of introduction, and the ability to control the number of founders. Such experimental introductions have provided some of the strongest empirical evidence of rapid phenotypic differentiation across a range of organisms, including anole lizards (Calsbeek & Cox, 2010 ; Kolbe et al., 2012 ; Losos et al., 2004 ; Stuart et al., 2014 ), peppered moths (Cook et al., 2012 ; Cook & Saccheri, 2013 ), and Trinidadian guppies (Reznick & Travis, 2019 ), but less research has focused on describing the underlying genetic architecture (although see Fraser et al., 2015 ; Whiting et al., 2022 ; van der Zee et al., 2022 ).…”

“…Identifying genomic signals of selection therefore requires describing the genomic diversity and past demography of the introduced population. The short time‐scale at which these demographic events occur complicates the use of genetic demographic inference methods (Epps & Keyghobadi, 2015 ; van der Zee et al., 2022 ), but the distribution of genetic polymorphisms within and among populations contains information about population bottlenecks and expansions.…”

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

“…Interestingly, the window on chr1 (chr1:9791276–9798829) shows population loadings reflecting distinct phylogenetic axes of parallelism for Caroni drainage rivers (TAC/G/AP) and non‐Caroni rivers (O/MAD) (Figure S8). The window on chr15 (chr15:5028361–5050793) (Figure S9) has been demonstrated to evolve in parallel following experimental translocations of HP guppies to LP environments (van der Zee et al, 2022). Here we do not observe full parallelism, instead finding evidence of multi‐parallelism indicative of multiple LP haplotypes segregating and experiencing selection among all rivers.…”

Extensive variation in germlinede novomutations inPoecilia reticulata

“…Overall, our estimate of the germline DNM rate, 1.35 ×10 −8 , is roughly comparable to estimates of other vertebrate species (Fig 3; Table S10), suggesting that rapid DNMs may not be the primary locus of selection in rapidly adaptive guppy populations. Indeed, relatively few sites in the guppy genome exhibit evidence of the hard sweeps associated with recent DNMs (Fraser et al, 2015), and patterns are more consistent with soft sweeps on standing genetic variation (van der Zee et al, 2022).…”

“…Alternatively, rapid adaptation could be a product of selection on standing genetic variation (Barrett & Schluter, 2008), and consistent with this, natural populations of guppies exhibit extensive genetic and phenotypic polymorphism (Almeida et al, 2020; Lin et al, 2022; Whiting et al, 2021, 2022). The role of DNMs versus standing genetic variation in the rapid adaptation of guppies has important implications to the locus and nature of evolution in this key ecological model, as well as molecular signature we might expect to detect from.…”