C. Garcia de Leaniz

A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation

Here we critically review the scale and extent of adaptive genetic variation in Atlantic salmon (Salmo salar L.), an important model system in evolutionary and conservation biology that provides fundamental insights into population persistence, adaptive response and the effects of anthropogenic change. We consider the process of adaptation as the end product of natural selection, one that can best be viewed as the degree of matching between phenotype and environment. We recognise three potential sources of adaptive variation: heritable variation in phenotypic traits related to fitness, variation at the molecular level in genes influenced by selection, and variation in the way genes interact with the environment to produce phenotypes of varying plasticity. Of all phenotypic traits examined, variation in body size (or in correlated characters such as growth rates, age of seaward migration or age at sexual maturity) generally shows the highest heritability, as well as a strong effect on fitness. Thus, body size in Atlantic salmon tends to be positively correlated with freshwater and marine survival, as well as with fecundity, egg size, reproductive success, and offspring survival. By contrast, the fitness implications of variation in behavioural traits such as aggression, sheltering behaviour, or timing of migration are largely unkown. The adaptive significance of molecular variation in salmonids is also scant and largely circumstantial, despite extensive molecular screening on these species. Adaptive variation can result in local adaptations (LA) when, among other necessary conditions, populations live in patchy environments, exchange few or no migrants, and are subjected to differential selective pressures. Evidence for LA in Atlantic salmon is indirect and comes mostly from ecological correlates in fitness‐related traits, the failure of many translocations, the poor performance of domesticated stocks, results of a few common‐garden experiments (where different populations were raised in a common environment in an attempt to dissociate heritable from environmentally induced phenotypic variation), and the pattern of inherited resistance to some parasites and diseases. Genotype × environment interactions occurr for many fitness traits, suggesting that LA might be important. However, the scale and extent of adaptive variation remains poorly understood and probably varies, depending on habitat heterogeneity, environmental stability and the relative roles of selection and drift. As maladaptation often results from phenotype‐environment mismatch, we argue that acting as if populations are not locally adapted carries a much greater risk of mismanagement than acting under the assumption for local adaptations when there are none. As such, an evolutionary approach to salmon conservation is required, aimed at maintaining the conditions necessary for natural selection to operate most efficiently and unhindered. This may require minimising alterations to native genotypes and habitats to which populations have likely become adapted, but also allowing for population size to reach or extend beyond carrying capacity to encourage competition and other sources of natural mortality.

Mitochondrial DNA variation in Pleistocene and modern Atlantic salmon from the Iberian glacial refugium

Current understanding of the postglacial colonization of Nearctic and Palearctic species relies heavily on inferences drawn from the phylogeographic analysis of contemporary generic variants. Modern postglacial populations are supposed to be representative of their Pleistocene ancestors, and their current distribution is assumed to reflect the different colonization success and dispersal patterns of refugial lineages. Yet, testing of phylogeographic models against ancestral genomes from glacial refugia has rarely been possible. Here we compare ND1 mitochondrial DNA variation in late Pleistocene (16 000–40 000 years before present), historical and contemporary Atlantic salmon (Salmo salar) populations from northern Spain and other regions of western Europe. Our study demonstrates the presence of Atlantic salmon in the Iberian glacial refugium during the last 40 000 years and points to the Iberian Peninsula as the likely source of the most common haplotype within the Atlantic lineage in Europe. However, our findings also suggest that there may have been significant changes in the genetic structure of the Iberian refugial stock since the last ice age, and question whether modern populations in refugial areas are representative of ice age populations. A common haplotype that persisted in the Iberian Peninsula during the Pleistocene last glacial maximum is now extremely rare or absent from European rivers, highlighting the need for caution when making phylogeographic inferences about the origin and distribution of modern genetic types.

From best to pest: changing perspectives on the impact of exotic salmonids in the southern hemisphere

Exotic salmonids were deliberately introduced to the southern hemisphere during the last part of the 20th century, initially to boost sport fishing and later to develop an aquaculture industry. Early introductions were justified by governments on purely utilitarian arguments as it was felt that translocated salmonids would capitalize on otherwise ‘underutilized’ aquatic niches. A century later, exotic salmonids are established in nearly all places where they were originally introduced and beyond, and constitute one of the main threats to endemic fish fauna, amongst which galaxiid fishes have perhaps been impacted the most. We screened the literature to document the changing perspectives on exotic salmonids in the southern hemisphere, and employed SWOT analysis to assess the conservation prognosis of native galaxiids in the face of salmonid invasions. Our analysis indicates that opinions differ and contradictions abound as to how to prevent further salmonid encroachment. This is largely due to lack of information on the impact of exotics but, more importantly, because the problem is often approached merely from a socio-economic perspective. Sport fishermen, for example, actively support the stocking of rivers to enhance sport fisheries and argue in favour of considering established salmonids as part of the native biodiversity, but also want to see an end to salmonids escaping from fish farms. The salmon industry tends to stress the social and economic benefits brought about by aquaculture, but continues to demand the right to expand and self-regulate. Governments, on the other hand, have not always had consistent or clear policies on exotic salmonids, and have tended to favour some stakeholders and penalized others. Our analysis emphasizes the need to consider biologically meaningful time scales when assessing impacts on biodiversity, and stresses the need to anticipate shifts in public opinion and stakeholder support in conservation.

Maladaptation and phenotypic mismatch in hatchery-reared Atlantic salmon Salmo salar released in the wild

Changes in body shape, fluctuating asymmetry (FA) and crypsis were compared among Atlantic salmon Salmo salar fry kept as controls in captivity and those released and subsequently recaptured in the wild according to a before-after-control-impact (BACI) design. Hatchery fish that survived in the wild became more cryptic and displayed a much lower incidence of fin erosion and of asymmetric individuals than control fish kept in captivity. Significant differences in body shape were also apparent, and survivors had longer heads, thicker caudal peduncles and a more streamlined body shape than hatchery controls as early as 20 days following stocking, most likely as a result of phenotypic plasticity and non-random, selective mortality of maladapted phenotypes. Hatchery-reared fish typically perform poorly in the wild and the results of this study indicate that this may be due to phenotypic mismatch, i.e. because hatcheries generate fish that are phenotypically mismatched to the natural environment.

The male handicap: male-biased mortality explains skewed sex ratios in brown trout embryos

Juvenile sex ratios are often assumed to be equal for many species with genetic sex determination, but this has rarely been tested in fish embryos due to their small size and absence of sex-specific markers. We artificially crossed three populations of brown trout and used a recently developed genetic marker for sexing the offspring of both pure and hybrid crosses. Sex ratios (SR = proportion of males) varied widely one month after hatching ranging from 0.15 to 0.90 (mean = 0.39 ± 0.03). Families with high survival tended to produce balanced or male-biased sex ratios, but SR was significantly female-biased when survival was low, suggesting that males sustain higher mortality during development. No difference in SR was found between pure and hybrid families, but the existence of sire × dam interactions suggests that genetic incompatibility may play a role in determining sex ratios. Our findings have implications for animal breeding and conservation because skewed sex ratios will tend to reduce effective population size and bias selection estimates.