Atlantic salmon (Salmo solar, Salmonidae) show a diversity of life history, behavioural and morphological adaptations for reproduction which have evolved as an outcome of competition to maximize reproductive success. Reproductive traits of females have been shaped principally by natural selection for offspring production and survival, those of males by sexual selection for access to matings. Female Atlantic salmon invest approximately six times more energy in offspring production (i.e. gonads) than males and face an important trade-off between number and size of eggs to produce that will maximize the number of surviving offspring. Timing of breeding and the construction of nests appear adapted to increase offspring survival. The most important determinant of female breeding success is body size because it affords high fecundity, access to breeding territories and decreased probability of nest destruction. Asynchronous female spawning and the male ability to spawn rapidly and repeatedly results in male-biased operational sex ratios that generate intense male competition for mates. This has likely been responsible for the evolution of elaborate male secondary sexual characters associated with fighting and status signalling. Furthermore, it has given rise, through frequency-dependent selection, to two alternative male breeding phenotypes: (1) large, anadromous males; and (2) small, mature male parr. Anadromous males invest heavily in behavioural activity on the spawning grounds, searching and fighting for mates and courting them, with body size being an important determinant of their breeding success. This behavioural activity carries a heavy cost, as anadromous males have significantly reduced survival relative to females. In contrast, mature male parr invest proportionally more in testes for sperm competition and attempt to ‘sneak’ access to matings. While this behaviour also carries costs in terms of subsequent growth and survival, male parr are more likely to breed again, either prior to or following a migration to sea, than anadromous males. While knowledge about the breeding of Atlantic salmon is detailed, we are only beginning to understand the ultimate causes and/or functional significances of their reproductive strategies. Predictive models of the life history variation are developing, focusing on the need for empirical study and testing of life history and reproductive patterns.

Reproductive strategies of Atlantic salmon: ecology and evolution

Genetic stochasticity due to small population size contributes to population extinction, especially when population fragmentation disrupts gene flow. Estimates of effective population size (Ne) can therefore be informative about population persistence, but there is a need for an assessment of their consistency and informative relevance. Here we review the body of empirical estimates of Ne for wild populations obtained with the temporal genetic method and published since Frankham's (1995) review. Theoretical considerations have identified important sources of bias for this analytical approach, and we use empirical data to investigate the extent of these biases. We find that particularly model selection and sampling require more attention in future studies.

We report a median unbiased Ne estimate of 260 (among 83 studies) and find that this median estimate tends to be smaller for populations of conservation concern, which may therefore be more sensitive to genetic stochasticity. Furthermore, we report a median Ne/N ratio of 0.14, and find that this ratio may actually be higher for small populations, suggesting changes in biological interactions at low population abundances. We confirm the role of gene flow in countering genetic stochasticity by finding that Ne correlates strongest with neutral genetic metrics when populations can be considered isolated. This underlines the importance of gene flow for the estimation of Ne, and of population connectivity for conservation in general. Reductions in contemporary gene flow due to ongoing habitat fragmentation will likely increase the prevalence of genetic stochasticity, which should therefore remain a focal point in the conservation of biodiversity.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-294X.2008.03842.x

Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence?

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 unknown. 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 x 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.

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

According to the theory of mate choice based on heterozygosity, mates should choose each other in order to increase the heterozygosity of their offspring. In this study, we tested the 'good genes as heterozygosity' hypothesis of mate choice by documenting the mating patterns of wild Atlantic salmon (Salmo salar) using both major histocompatibility complex (MHC) and microsatellite loci. Specifically, we tested the null hypotheses that mate choice in Atlantic salmon is not dependent on the relatedness between potential partners or on the MHC similarity between mates. Three parameters were assessed: (i) the number of shared alleles between partners (x and y) at the MHC (M(xy)), (ii) the MHC amino-acid genotypic distance between mates' genotypes (AA(xy)), and (iii) genetic relatedness between mates (r(xy)). We found that Atlantic salmon choose their mates in order to increase the heterozygosity of their offspring at the MHC and, more specifically, at the peptide-binding region, presumably in order to provide them with better defence against parasites and pathogens. This was supported by a significant difference between the observed and expected AA(xy) (p = 0.0486). Furthermore, mate choice was not a mechanism of overall inbreeding avoidance as genetic relatedness supported a random mating scheme (p = 0.445). This study provides the first evidence that MHC genes influence mate choice in fish.

/pdf/good-genes-as-heterozygosity-the-major-histocompatibility-33vgi67jim.pdf

'Good genes as heterozygosity': the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar).

Geir Lasse Taranger1, Orjan Karlsen2*, Raymond John Bannister1, Kevin Alan Glover1, Vivian Husa1, Egil Karlsbakk1, Bjorn Olav Kvamme1, Karin Kroon Boxaspen1, Pal Arne Bjorn3, Bengt Finstad4, Abdullah Sami Madhun1, H. Craig Morton1, and Terje Svasand1 Institute of Marine Research, PB 1870, N-5817 Bergen, Norway Institute of Marine Research, Austevoll Research Station, N-5392 Storebo, Norway Institute of Marine Research, PB 6404, N-9294 Tromso, Norway Norwegian Institute for Nature Research, PB 5685 Sluppen, N-7485 Trondheim, Norway *Corresponding author: tel: +47 4691 2740; fax: +47 5618 2222; e-mail: OrjanK@imr.no

Risk assessment of the environmental impact of Norwegian Atlantic salmon farming

Summary
(1) Based on data from the literature, the phenomenon of homing in salmonids is examined with special reference to the Atlantic salmon. Wild, native fish demonstrate an excellent homing ability, judged from percent return to the home river (1–3 %) and straying to non-native watersheds (less than 3 % of returning fish).

(2) The homing ability in wild fish is shown to be closely related to the existence of reproductively isolated populations between and within watersheds, as demonstrated by data from salmonid ecology and biochemical genetics.

(3) Two main hypotheses have dominated the literature on salmonid homing during recent years: (a) An ‘imprinting’ hypothesis based on a process of learning of stream odours during seaward migration, coupled with sun-orientation for open sea navigation, (b) A ‘pheromone’ hypothesis related to odours from fish and based on inheritance and the seasonal migrating schedules of discrete populations.

(4) The olfactory sense has been demonstrated as mandatory for salmonids, both in near range and open sea navigation. According to genetic, sensory and ecological aspects of homing, the pheromone hypothesis is therefore concluded to be the most appropriate.

(5) Fish produced from artificially fertilized eggs, released within native systems or transplanted, demonstrate a reduced homing ability. Since hatchery-raised fish demonstrate a survival in sea equivalent to that of wild fish, a genetic disturbance of navigational ability has been suggested, resulting from the production of population hybrids by man.

(6) Studies made in the fields of behaviour, electrophysiology and chemistry strongly suggest that population-specific fish odours are involved in home-stream recognition by salmonids.

(7) An evaluation of ‘imprinting’ experiments related to artificial organic compounds reveals that: (a) the odorant properties of the applied chemicals must be questioned, (b) imprinting related to olfaction may be based on a weak theoretical foundation, (c) returns obtained in census experiments may be adequately explained through ecological interpretations, and (d) behavioural preferences obtained from exposure to non-natural compounds may be founded on mechanisms not associated with homing.

(8) A logical link between the use of olfaction and the role of genetics in salmonid homing is emphasized, together with its practical implications for salmonid management.

Homing and olfaction in salmonids: a critical review with special reference to the atlantic salmon

Attraction and preference behavior patterns shown by Atlantic salmon (Salmo salar L.) parr towards intraspecific odors were measured. Salmon parr were attracted to tank water in which relatives of their own strain were held but were also attracted to tank water containing another strain of their species. When given a choice between the two types of tank water, water containing their own strain odor was significantly favored over water containing conspecific but nonfamiliar odor, revealing that pheromones are present at intraspecific levels in salmonid juveniles. Competitive experiments with various extracts suggest that the active compounds are most likely produced in the liver and are voided via the intestinal tract, as determined by presence of attractants in intestinal contents and bile. Intraspecific discrimination was not detected with extracts from either skin surface mucus or blood plasma. Extracts from gravel that had been kept below the fish in their rearing tanks, however, induced a strain-related preference behavior. This suggests an ability for substrate marking by salmonid fishes, presumably mediated by deposition of fecal material. Strain discrimination and substrate marking are discussed in relation to stationary behavior and homing of fishes within discrete populations in natural systems.

Intraspecific pheromone discrimination and substrate marking by atlantic salmon parr.

A new method for collecting non-contaminated skin mucus from fishes is introduced. The method is compared with a "customary" method by gel filtration, analysis of free amino acids, and determination of dry weight. Skin mucus collected by the "customary" method is shown to be contaminated by intestinal juice. The role of skin mucus as a source of fish odorants affecting fish behaviour is discussed in the light of the above findings.

Comparison of mucus collecting methods in fish olfaction.

Samples of skin mucus and intestinal contents were collected from groups of salmon presmolt from three Norwegian rivers. The supernatants obtained after precipitation were gel-filtered on a Sephadex G-25 column, which revealed peaks with absorption at 280 nm. Fractions incorporating a group of retarded peaks were examined by two-dimensional thin-layer chromatography. The spots obtained on the thin-layer plates were sorted out by means of position, intensity, and fluorescence properties.R

 f
 values for the assumed identical spots from each group were subjected to statistical analysis. In one of the chromatography systems, 8 spots of 24 from samples of skin mucus and 6 spots of 27 from intestinal contents show larger standard deviations (SD) ofR

 f
 than may be expected when a substance is chromatographed repeatedly. These SDs fit a linear relationship of SD to chromatography length by a probability of less than 0.01. The results indicate a molecular variation between the groups which could be a source for population-specific odorants. If these substances are used in chemical communication, they can provide the specific clues needed for a successful return to the home river.

Ole B. Stabell

Papers

Homing and olfaction in salmonids: a critical review with special reference to the atlantic salmon

Intraspecific pheromone discrimination and substrate marking by atlantic salmon parr.

Comparison of mucus collecting methods in fish olfaction.

A comparative chemical study on population-specific odorants from atlantic salmon.

A note on the significance of the olfactory sense upon sexual maturation in Atlantic salmon (Salmo salar L.)