Parallel Evolution and Vicariance in the Guppy (Poecilia Reticulata) Over Multiple Spatial and Temporal Scales

Abstract

Well-studied model systems present ideal opportunities to understand the relative roles of contemporary selection versus historical processes in determining population differentiation and speciation. Although guppy populations in Trinidad have been a model for studies of evolutionary ecology and sexual selection for more than 50 years, this work has been conducted with little understanding of the phylogenetic history of this species. We used variation in nuclear (X-src) and mitochondrial DNA (mtDNA) sequences to examine the phylogeographic history of Poecilia reticulata Peters (the guppy) across its entire natural range, and to test whether patterns of morphological divergence are a consequence of parallel evolution. Phylogenetic, nested clade, population genetic, and demographic analyses were conducted to investigate patterns of genetic structure at several temporal scales and are discussed in relation to vicariant events, such as tectonic activity and glacial cycles, shaping northeast South American river drainages. The mtDNA phylogeny defined five major lineages, each associated with one or more river drainages, and analysis of molecular variance also detected geographic structuring among these river drainages in an evolutionarily conserved nuclear (X-src) locus. Nested clade and other demographic analyses suggest that the eastern Venezuela/ western Trinidad region is likely the center of origin of P. reticulata. Mantel tests show that the divergence of morphological characters, known to differentiate on a local scale in response to natural and sexual selection pressures, is not associated with mtDNA genetic distance; however, TreeScan analysis identified several significant associations of these characters with the haplotype tree. Parallel upstream/downstream patterns of morphological adaptation in response to selection pressures reported in P. reticulata within Trinidad rivers appears to persist across the natural range. Our results together with previous studies suggest that, although morphological variation in P. reticulata is primarily attributed to selection, phylogeographic history may also play a role.

Microsatellite genetic differentiation among populations of the Trinidadian guppy

“…We found higher levels of genetic diversity and population subdivision than has been previously reported in studies based on allozymes Shaw et al, 1991Shaw et al, , 1992 and mtDNA (Fajen and Breden, 1992;Alexander et al, 2006). Microsatellites are particularly useful in the study of fine-scale genetic structure because of high mutation rates and levels of polymorphism.…”

“…Our data do not provide compelling support for previous claims of two major genetic lineages of guppies in northern Trinidad. Earlier studies postulated that the guppies in northern Trinidad were differentiated between the Caroni and Oropouche drainages, and that the populations from northern rivers clustered with the Caroni drainage (Boos, 1984;Fajen and Breden, 1992;Alexander et al, 2006). These studies suggested that there were two major colonization events associated with the two drainages.…”

“…First, studies using allozymes or mtDNA have revealed marked genetic divergence between populations from two major drainages, the Caroni, which drains west into the Gulf of Paria, and the Oropouche, which flows east into the Atlantic Ocean (Figure 1; Carvalho et al, 1991;Shaw et al, 1991Shaw et al, , 1994Fajen and Breden, 1992;Alexander et al, 2006). Differentiation between the two drainages supports the 'two arcs' hypothesis, which asserts that the freshwater fauna in the Caroni (including northernflowing rivers along the northern coast) and Oropouche drainages derive from different ancestral lineages (Boos, 1984).…”

“…Differentiation between the two drainages supports the 'two arcs' hypothesis, which asserts that the freshwater fauna in the Caroni (including northernflowing rivers along the northern coast) and Oropouche drainages derive from different ancestral lineages (Boos, 1984). Specifically, during the Pleistocene era, sea levels were up to 130 m lower than at present (Kenny, 1989) and parts of the Orinoco river system-the major river system running through Venezuela-discharged northward and into the Gulf of Paria, and probably created confluences with the present-day Caroni drainage and several rivers along the northern coast of Trinidad (Ingman et al, 2000;Alexander et al, 2006). Conversely, the Oropouche drainage likely had confluences with a different drainage system on mainland South America and would have been exposed to different colonizing events.…”

Genetically and environmentally mediated divergence in lateral line morphology in the Trinidadian guppy (Poecilia reticulata)

“…A suite of environmental factors covaries with predation pressure, and the multivariate nature of these environments results in a diversity of selection pressures that may directly or indirectly influence neuromast distribution. For example, differences in food availability and food types Zandonà et al, 2011), water flow characteristics , body shape (Alexander et al, 2006) and developmental timing (e.g. Reznick et al, 1990;Arendt and Reznick, 2005) between high-and lowpredation populations could contribute to changes in neuromast number and distribution (Rosen and Mendelson, 1960;Münz, 1979;Coombs et al, 1992;Levin, 2010).…”