Leif Asbjørn Vøllestad

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.

Genetic divergence and phylogeographic relationships among european perch (Perca fluviatilis) populations reflect glacial refugia and postglacial colonization.

We used the widely distributed freshwater fish, perch (Perca fluviatilis), to investigate the postglacial colonization routes of freshwater fishes in Europe. Genetic variability within and among drainages was assessed using mitochondrial DNA (mtDNA) D‐loop sequencing and RAPD markers from 55 populations all over Europe as well as one Siberian population. High level of structuring for both markers was observed among drainages and regions, while little differentiation was seen within drainages and regions. Phylogeographic relationships among European perch were determined from the distribution of 35 mtDNA haplotypes detected in the samples. In addition to a distinct southern European group, which includes a Greek and a southern Danubian population, three major groups of perch are observed: the western European drainages, the eastern European drainages including the Siberian population, and Norwegian populations from northern Norway, and western side of Oslofjord. Our data suggest that present perch populations in western and northern Europe were colonized from three main refugia, located in southeastern, northeastern and western Europe. In support of this, nested cladistic analysis of mtDNA clade and nested clade distances suggested historical range expansion as the main factor determining geographical distribution of haplotypes. The Baltic Sea has been colonized from all three refugia, and northeastern Europe harbours descendants from both eastern European refugia. In the upper part of the Danube lineages from the western European and the southern European refugia meet. The southern European refugium probably did not contribute to the recolonization of other western and northern European drainages after the last glaciation. However, phylogenetic analyses suggest that the southern European mtDNA lineage is the most ancient, and therefore likely to be the founder of all present perch lineages. The colonization routes used by perch probably also apply to other freshwater species with similar distribution patterns.

A meta-analysis of fluctuating asymmetry in relation to heterozygosity

Fluctuating asymmetry, the random departure from perfect bilateral symmetry, is a common measure of developmental instability that has been hypothesized to be inversely correlated with heterozygosity. Although this claim has been widely repeated, several studies have reported no such association. Therefore, we test the generality of this association, using meta-analysis, by converting test statistics for the relationship between heterozygosity (H) and fluctuating asymmetry (FA) into a common effect size, the Pearson’s product-moment correlation coefficient. We have analysed a database containing 41 studies with a total of 118 individual samples. Overall we found an unweighted mean negative effect size; r=−0.09 (i.e. a negative correlation between H and FA). Significant heterogeneity in effect size was mainly caused by a difference between ectothermic and endothermic animals, and to a lesser extent by the use of different study designs (i.e. within-population vs. among-populations). Mean effect size for endothermic animals was positive and significantly different from the mean effect size for ectothermic animals. Only for within-population studies of ectothermic animals did we find a significantly negative effect size (r=−0.23 ± 0.09). The distribution of effect sizes in relation to sample size provided little evidence for patterns typical of those produced by publication bias. Our analysis suggests, at best, only a weak association between H and FA, and heterozygosity seems to explain only a very small amount of the variation in developmental instability among individuals and populations (r2=0.01 for the total material).

Population differences in early life‐history traits in grayling

In this paper we test population differences in early life‐history traits in three grayling Thymallus thymallus populations. The grayling shared ancestors some 80–90 years ago. We performed common‐garden experiments at three temperatures (mimicking population‐specific summer temperatures), and measured survival and growth rates during early development. We found significant additive genetic variance in size (length and yolk‐sac volume) measured at hatching, swim‐up and termination of the experiment, and significantly different reaction norms for growth rate and survival during the period of first feeding. In general, each population did best at the temperature experienced in nature. These differences in early life‐history traits suggest that natural selection has resulted in local adaptation in a time period of 13–18 generations.

LATITUDINAL VARIATION IN LIFE‐HISTORY TRAITS IN EURASIAN PERCH

Few studies have examined multiple life-history traits across a latitudinal gradient to test whether variation in growth rate and mortality schedules induces trends predicted by life-history theory. We collected data for the following life-history traits for 75 Eurasian perch (Perca fluviatilis) populations: growth coefficient (K) and asymptotic body length (L∞) from the von Bertalanffy growth model, size at ages one and two years, specific juvenile growth rate, instantaneous adult and juvenile mortality rates, life span, age and length at maturity, and reproductive life span and investment. All life-history traits except L∞ were significantly correlated with latitude. In general, growth rates, mortality rates, and reproductive investment decreased with latitude, whereas age at maturity, size at maturity, and life span increased with latitude. Populations could be grouped into two categories based on variation in L∞: stunted (small sized) vs. piscivorous (large sized). Four trait–latitude relationships di...

A century of life-history evolution in grayling

Synchronic and allochronic data sets consisting of phenotypic values of various life-history traits from five grayling Thymallus thymallus populations with common ancestors were analysed for the purpose of estimating evolution and divergence rates. The synchronic data contained both juvenile and adult traits from populations that have been segregated for 44-88 years (9-22 generations). The allochronic time series contained growth- and maturation data spanning 95 years (16 generations). Estimated evolution and divergence rates were high compared with other life-history studies on the same temporal scale (0.002-1.008 haldanes, 10-30, 500 darwins). The divergence of adult traits were most probably caused by differential mortalities induced by variation in fishing intensity. For the population with allochronic data, 48 years (eight generations) of intense and consistent size-selective gillnet fishing resulted in a constant reduction in age (-0.33 years pr 10 year) and length (-18 mm pr 10 year) at maturity. Length-at-age for ages one to five also decreased during the same period. When gill-net fishing was relaxed, age and length at maturity and length-at-age increased. Divergence rates for juvenile traits derived from a common-garden experiment were high, and standardized selection differentials (s′) were high, especially for yolk-sac volume (s′ = 2.6). We also document that low divergence rates for juvenile traits were lower between populations having similar spawning/nursery habitats (running water) than populations having relatively different habitats (running water v.s. still water). We suggest that the major part of the observed phenotypic divergence is mostly due to adaptive evolution, although microsatellite data indicate that genetic drift also has occurred.

Life-History Characteristics of the European Eel Anguilla anguilla in the Imsa River, Norway

Abstract Each summer between June and September, elvers (6.4–9.0 cm total length) and a small number of yellow (12–26 cm) European eels ascend the Imsa River. In fresh water, the mean annual length increment from the elver stage to age 8 years was 6.2 cm. Males grew more slowly than females in the corresponding year classes. The male:female ratio was approximately 1:20. Male and female yellow European eels transformed into silver eels at lengths of about 40 cm and 62 cm, respectively. Rapidly growing eels of both sexes transformed into silver eels at younger ages than more slowly growing individuals. Length was more important than age for the onset of transformation. Length-weight relationships indicated that growth was allometric and that silver eels were heavier than yellow eels of the same length. Gonad weight of the females increased exponentially with body length, whereas the mean gonadosomatic index, gonad weight/(total weight - gonad weight), did not vary with length.

An Evaluation of Visible Implant Elastomer for Marking Age-0 Brown Trout

Abstract Injection of visible implant elastomer (VIE) was evaluated as a way to provide age-0 brown trout Salmo trutta with externally visible internal marks. We first tested this fluorescent elastomer material in a laboratory experiment using a single color and body position to batch-mark the fish (28.9–44.1 mm fork length). The experiment lasted for 77 d, with no mortality or tag loss and no significant (P = 0.44) effect on fish growth. Similar marks were then used to individually tag age-0 brown trout (26–70 mm) in small streams in the wild using four different colors and several body positions. The immediate mortality associated with the marking procedure was low (0.5%), and visual identification of VIE marks on recaptured individuals (169 out of 699 released; 39–83 d between release and recapture) was not difficult. We found no significant differences in mean fork length between tagged and untagged individuals captured on the same date at given sampling locations. This suggests that capture and marki...

Trade-off between growth rate and aggression in juvenile coho salmon, Oncorhynchus kisutch

In juvenile salmon and trout, there seems to be a positive phenotypic correlation between individual aggression level and growth rate. Aggressive fish are dominant, and they obtain and defend territories, giving them access to good feeding sites. Being aggressive may increase predation risk, and may also carry costs such as increased metabolic demand, with effects on growth. To test the hypothesis that there is a trade-off between individual growth rate and aggression, we mated 12 female coho salmon with two unique males each, creating 24 full-sibling families. Growth of individually marked fish from each family was estimated in a situation where food could not be monopolized. Thereafter, individual fish were tested for mirror-elicited agonistic behaviour. We found significant variation between families in early growth rate, with a high heritability (1.04). There was also significant between-family variation in agonistic behaviour, but activity was generally low and heritability was low (0.25) and not significant. Growth rate and agonistic behaviour were negatively correlated. These results imply that aggressive behaviour has an energetic cost. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

Permanent impairment in the feeding behavior of grayling (Thymallus thymallus) exposed to methylmercury during embryogenesis.

Embryos of grayling (Thymallus thymallus) were exposed to different concentrations of methylmercury (0.16, 0.8, 4.0 and 20 micrograms Hg l-1) during the first 10 days of development. The exposure resulted in body concentrations in the newly hatched fry of 0.09, 0.27, 0.63 and 3.80 micrograms Hg g-1 wet wt., respectively. A control group had a body concentration of 0.01 microgram Hg g-1. Morphological disturbances were only found in the highest exposure group. Three years later, at a size of 13.8 +/- 0.8 cm, the different groups were tested for sublethal toxicant effects on foraging behavior. In the first series of experiments we tested the foraging efficiency of the fish when kept alone for 5 min in small flow-through aquariums. In the second series of experiments we tested the competitive ability of eight individuals from an exposed group vs. eight individuals from a control group when kept together for 30 min in a 300-1 aquarium. In both experiments live Dapnia magna were used as prey. We found impaired feeding efficiencies and reduced competitive abilities in grayling from the exposed groups which as yolk-fry had Hg concentrations of 0.27 microgram g-1 or more. In the foraging efficiency experiments these groups were 15-24% less efficient as compared to the control group. In the competitive ability experiments the control group caught two to six times as many preys as these exposed groups. Such harmful body concentrations of Hg (> 0.27 microgram g-1) may be found in eggs from piscivorous fishes in lakes receiving diffuse atmospheric depositions of mercury. We suggest such concentrations may have ecological consequences by reducing the fitness of the affected populations.