Population structure of guppies in north-eastern Venezuela, the area of putative incipient speciation.

BACKGROUND: Geographic barriers to gene flow and divergence among populations in sexual traits are two important causes of genetic isolation which may lead to speciation. Genetic isolation may be facilitated if these two mechanisms act synergistically. The guppy from the Cumaná region (within the Cariaco drainage) of eastern Venezuela has been previously described as a case of incipient speciation driven by sexual selection, significantly differentiated in sexual colouration and body shape from the common guppy, Poecilia reticulata. The latter occurs widely in northern Venezuela, including the south-eastern side of Cordillera de la Costa, where it inhabits streams belonging to the San Juan drainage. Here, we present molecular and morphological analyses of differentiation among guppy populations in the Cariaco and San Juan drainages. Our analyses are based on a 953 bp long mtDNA fragment, a set of 15 microsatellites (519 fish from 20 populations), and four phenotypic traits. RESULTS: Both microsatellite and mtDNA data showed that guppies inhabiting the two drainages are characterised by a significant genetic differentiation, but a higher proportion of the genetic variance was distributed among populations within regions. Most guppies in the Cariaco drainage had mtDNA from a distinct lineage, but we also found evidence for widespread introgression of mtDNA from the San Juan drainage into the Cariaco drainage. Phenotypically, populations in the two regions differed significantly only in the number of black crescents. Phenotypic clustering did not support existence of two distinct groupings, but indicated a degree of distinctiveness of Central Cumaná (CC) population. However, CC population showed little differentiation at the neutral markers from the proximate populations within the Cariaco drainage. CONCLUSIONS: Our findings are consistent with only partial genetic isolation between the two geographic regions and indicate that the geographic barrier of Cordillera de la Costa has not played an important role in strengthening the incomplete pre-zygotic reproductive barrier between Cumaná and common guppy. Significant phenotypic differentiation between genetically similar (in terms of neutral variation) populations suggests that mate choice can maintain divergence at sexually selected traits despite gene flow. However, neither genetic nor phenotypic clustering supported delineation of two species within the region.

Variance components of sex determination in the copepod Tigriopus californicus estimated from a pedigree analysis.

Extensive theory exists regarding population sex ratio evolution that predicts equal sex ratio (when parental investment is equal). In most animals, sex chromosomes determine the sex of offspring, and this fixed genotype for sex has made theory difficult to test since genotypic variance for the trait (sex) is lacking. It has long been argued that the genotype has become fixed in most animals due to the strong selection for equal sex ratios. The marine copepod Tigriopus californicus has no sex chromosomes, multiple genes affecting female brood sex ratio, and a brood sex ratio that responds to selection. The species thus provides an opportune system in which to test established sex ratio theory. In this paper, we further our exploration of polygenic sex determination in T. californicus using an incomplete diallel crossing design for analysis of the variance components of sex determination in the species. Our data confirm the presence of extra-binomial variance for sex, further confirming that sex is not determined through simple Mendelian trait inheritance. In addition, our crosses and backcrosses of isofemale lines selected for biased brood sex ratios show intermediate phenotypic means, as expected if sex is a threshold trait determined by an underlying "liability" trait controlled by many genes of small effects. Furthermore, crosses between families from the same selection line had similar increases in phenotypic variance as crosses between families from different selection lines, suggesting families from artificial selection lines responded to selection pressure through different underlying genetic bases. Finally, we estimate heritability of an individual to be male or female on the observed binary scale as 0.09 (95% CI: 0.034-0.14). This work furthers our accumulating evidence for polygenic sex determination in T. californicus laying the foundation for this as a model species in future studies of sex ratio evolution theory.

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

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.

Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia.

High genetic diversity is thought to characterize successful invasive species, as the potential to adapt to new environments is enhanced and inbreeding is reduced. In the last century, guppies, Poecilia reticulata, repeatedly invaded streams in Australia and elsewhere. Quantitative genetic studies of one Australian guppy population have demonstrated high additive genetic variation for autosomal and Y-linked morphological traits. The combination of colonization success, high heritability of morphological traits, and the possibility of multiple introductions to Australia raised the prediction that neutral genetic diversity is high in introduced populations of guppies. In this study we examine genetic diversity at nine microsatellite and one mitochondrial locus for seven Australian populations. We used mtDNA haplotypes from the natural range of guppies and from domesticated varieties to identify source populations. There were a minimum of two introductions, but there was no haplotype diversity within Australian populations, suggesting a founder effect. This was supported by microsatellite markers, as allelic diversity and heterozygosity were severely reduced compared to one wild source population, and evidence of recent bottlenecks was found. Between Australian populations little differentiation of microsatellite allele frequencies was detected, suggesting that population admixture has occurred historically, perhaps due to male-biased gene flow followed by bottlenecks. Thus success of invasion of Australia and high additive genetic variance in Australian guppies are not associated with high levels of diversity at molecular loci. This finding is consistent with the release of additive genetic variation by dominance and epistasis following inbreeding, and with disruptive and negative frequency-dependent selection on fitness traits.