Hybridization between distant lineages increases adaptive variation during a biological invasion: stickleback in Switzerland

The three-spined stickleback is a widespread Holarctic species complex that radiated from the sea into freshwaters after the retreat of the Pleistocene ice sheets. In Switzerland, sticklebacks were absent with the exception of the far northwest, but different introduced populations have expanded to occupy a wide range of habitats since the late 19th century. A well-studied adaptive phenotypic trait in sticklebacks is the number of lateral plates. With few exceptions, freshwater and marine populations in Europe are fixed for either the low plated phenotype or the fully plated phenotype, respectively. Switzerland, in contrast, harbours in close proximity the full range of phenotypic variation known from across the continent. We addressed the phylogeographic origins of Swiss sticklebacks using mitochondrial partial cytochrome b and control region sequences. We found only five different haplotypes but these originated from three distinct European regions, fixed for different plate phenotypes. These lineages occur largely in isolation at opposite ends of Switzerland, but co-occur in a large central part. Across the country, we found a strong correlation between a microsatellite linked to the high plate ectodysplasin allele and the mitochondrial haplotype from a region where the fully plated phenotype is fixed. Phylogenomic and population genomic analysis of 481 polymorphic amplified fragment length polymorphism loci indicate genetic admixture in the central part of the country. The same part of the country also carries elevated within-population phenotypic variation. We conclude that during the recent invasive range expansion of sticklebacks in Switzerland, adaptive and neutral between-population genetic variation was converted into within-population variation, raising the possibility that hybridization between colonizing lineages contributed to the ecological success of sticklebacks in Switzerland.

Invasion and fixation of sex-reversal genes

We simulated a meta-population with random dispersal among demes but local mating within demes to investigate conditions under which a dominant female-determining gene W, with no individual selection advantage, can invade and become fixed in females, changing the population from male to female heterogamety. Starting with one mutant W in a single deme, the interaction of sex ratio selection and random genetic drift causes W to be fixed among females more often than a comparable neutral mutation with no influence on sex determination, even when YY males have slightly reduced viability. Meta-population structure and interdeme selection can also favour the fixation of W. The reverse transition from female to male heterogamety can also occur with higher probability than for a comparable neutral mutation. These results help to explain the involvement of sex-determining genes in the evolution of sex chromosomes and in sexual selection and speciation.

Direct male-male competition can facilitate invasion of new colour types in Lake Victoria cichlids

The possibility that disruptive sexual selection alone can cause sympatric speciation is currently a subject of much debate. The initial difficulty for new and rare ornament phenotypes to invade a population, and the stabilisation of the resulting polymorphism in trait and preference make this hypothesis problematic. Recent theoretical work indicates that the invasion is facilitated if males with the new phenotype have an initial advantage in male-male competition. We studied a pair of sympatric incipient species of cichlids from Lake Victoria, in which the red (Pundamilia nyererei) and blue males (P. pundamilia) vigorously defend territories. Other studies suggested that red phenotypes may have repeatedly invaded blue populations in independent episodes of speciation. We hypothesised that red coloration confers an advantage in male-male competition, assisting red phenotypes to invade. To test this hypothesis, we staged contests between red and blue males from a population where the phenotypes are interbreeding morphs or incipient species. We staged contests under both white and green light condition. Green light effectively masks the difference between red and blue coloration. Red males dominated blue males under white light, but their competitive advantage was significantly diminished under green light. Contests were shorter when colour differences were visible. Experience of blue males with red males did not affect the outcome of a contest. The advantage of red over blue in combats may assist the red phenotype to invade blue populations. The apparently stable co-existence of red and blue incipient species in many populations of Lake Victoria cichlids is discussed.

Hybrid ‘superswarm’ leads to rapid divergence and establishment of populations during a biological invasion

Understanding the genetic background of invading species can be crucial information clarifying why they become invasive. Intraspecific genetic admixture among lineages separated in the native ranges may promote the rate and extent of an invasion by substantially increasing standing genetic variation. Here we examine the genetic relationships among threespine stickleback that recently colonized Switzerland. This invasion results from several distinct genetic lineages that colonized multiple locations and have since undergone range expansions, where they coexist and admix in parts of their range. Using 17 microsatellites genotyped for 634 individuals collected from 17 Swiss and two non-Swiss European sites, we reconstruct the invasion of stickleback and investigate the potential and extent of admixture and hybridization among the colonizing lineages from a population genetic perspective. Specifically we test for an increase in standing genetic variation in populations where multiple lineages coexist. We find strong evidence of massive hybridization early on, followed by what appears to be recent increased genetic isolation and the formation of several new genetically distinguishable populations, consistent with a hybrid ‘superswarm’. This massive hybridization and population formation event(s) occurred over approximately 140 years and likely fuelled the successful invasion of a diverse range of habitats. The implications are that multiple colonizations coupled with hybridization can lead to the formation of new stable genetic populations potentially kick-starting speciation and adaptive radiation over a very short time.

Cryptic invasion drives phenotypic changes in central European threespine stickleback

Cryptic invasions are commonly associated with genetic changes of the native species or genetic lineage that the invaders replace. Phenotypic shifts resulting from cryptic invasions are less commonly reported given the relative paucity of historical specimens that document such phenotypic changes. Here, I study such a case in two populations of threespine stickleback from central Europe, comparing contemporary patterns of gene flow with phenotypic changes between historical and contemporary population samples. I find gene flow from an invasive lineage to be associated with significant phenotypic changes, where the degree of phenotypic change corresponds with the level of gene flow that a population receives. These findings underline the utility of combining genetic approaches with phenotypic data to estimate the impact of gene flow in systems where anthropogenic alterations have removed former geographic barriers promoting cryptic invasions.