Molecular systematics of the genus Poecilia, and population structure and sexual selection in the guppy, Poecilia reticulata


Molecular systematics of the genus Poecilia

The genus Poecilia exhibits extensive morphological, behavioral, and life history variation within and between populations and between species.  This natural variation, coupled with short generation times and the ease with which members of this genus can be cultured in the lab, have made several species of Poecilia model systems for studying the effect of sexual and natural selection on the evolution of natural populations.  However, this work has been done without a well-resolved phylogeny, and this has limited the comparative work that could be done with this system.  For several years my major research effort has been directed toward producing a phylogeny of species and populations within this genus, in order to better understand the influence of natural and sexual selection in this group.

Parallel evolution and vicariance in the guppy (Poecilia reticulata) over multiple spatial and temporal scales

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 sequences to examine the phylogeographic history of guppy populations across the entire natural range, and to test whether patterns of morphological divergence are a consequence of parallel evolution. We used phylogenetic, nested clade, population genetic and demographic analyses to investigate patterns of genetic structure at several temporal scales, in relation to vicariant events, such as tectonic activity and glacial cycles, shaping northeast South American river drainages. Our mtDNA phylogeny defines four major lineages, each associated with one or more river drainages, and analysis of molecular variance (AMOVA) also shows geographic structuring among these river drainages in an evolutionarily conserved nuclear (X-src) locus. Nested clade analysis (NCA) and other demographic analyses suggest that the east Venezuela/west Trinidad region is likely the center of origin of P. reticulata. Parallel upstream/downstream patterns of morphological adaptation in response to selection pressures reported in 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.

Incipient speciation in the Cumaná guppy

Theory predicts that sexual selection can promote the evolution of reproductive isolation and speciation. Those cases in which sexual selection has led to speciation ought to be characterized by (1) significant differentiation in male display traits, (2) correlated differences in female preferences, (3) the absence of post-zygotic isolation, and (4) little genetic or other morphological differentiation. Previous evidence from our lab indicated that a cluster of populations of the guppy from Cumaná, Venezuela, known in the aquarium trade as Endler’s Livebearer, differs significantly in female preferences from nearby guppy populations, leading to sexual isolation between these populations. In addition, these populations exhibit significant divergence in male display traits correlated to differences in between-population mating success, little mitochondrial genetic differentiation, and we found no evidence for genetic incompatibility between a Cumaná population and several geographically isolated “standard” populations. These results suggest that divergent sexual selection has contributed to differentiation of the Cumaná guppy, and that this may be the first example of incipient speciation in the guppy.  We are now conducting microsatellite analysis of these populations, and examining variation in opsin genes as candidates for driving differentiation and speciation.