Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies

Abstract

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.

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

“…PC3 and PC4 did not further separate populations and all other PCs accounted for <5% of the variation (figure S1). When compared to natural populations across the Northern Range described in Whiting et al (2020), the experimental populations show very limited divergence from their source (GHP) (figure S2). Pairwise F ST was low between introduced populations and their source (median F ST = 0.013 – 0.023), with the strongest difference found between IT and GHP (table S2).…”

“…This region has previously been identified as a candidate for convergent evolution in natural populations and long-term experimental populations, in a RADSeq study (specifically in the Oropuche, Arima, and introduction Aripo HP-LP pairs) (Fraser et al 2015). Further, using whole-genome sequencing, this same region was found to be a candidate of selection in the Tacarigua and Oropuche population pairs and a region slightly upstream in the Aripo and Tacarigua pairs (Whiting et al 2020). Finally, the cadherin signaling pathway was enriched for signatures of selection in all paired comparisons of HP and LP populations studied (Whiting et al 2020).…”

“…Further, using whole-genome sequencing, this same region was found to be a candidate of selection in the Tacarigua and Oropuche population pairs and a region slightly upstream in the Aripo and Tacarigua pairs (Whiting et al 2020). Finally, the cadherin signaling pathway was enriched for signatures of selection in all paired comparisons of HP and LP populations studied (Whiting et al 2020). Cadherin family genes are known to be involved in pigment cell migration and other cell-cell adhesion processes (Fukuzawa and Obika 1995; Nishimura et al 1999), and could thus be involved in the colour differences between HP and LP males.…”

“…Principal component analysis with natural populations described in (Whiting et al, 2020) illustrating the lack of population structure between GHP and the introduced populations.…”

Substantial intraspecific variation in energy budgets: biology or artefact?

“…The distinction between guppy ecotypes is well characterised (Reznick and Endler, 1982;Reznick, 1982;Reznick and Bryga, 1987). However, there is substantial life-history variation among low-predation populations from different streams, including differences in rates of senescence (Reznick et al, 2004(Reznick et al, , 2005, juvenile growth rates (Arendt and Reznick, 2005), basal metabolic rate (Auer et al, 2018), how competitive ability scales with body size (Potter et al, 2019), and in genes associated with living in a low-predation habitat (Whiting et al, 2020). Our results here support the notion that there are multiple mechanistic routes through which the low-predation ecotype can evolve.…”