Thermal variability induces sex-specific morphometric changes in zebrafish (Danio rerio).

In nature, organisms are exposed to variable environmental conditions that impact their performance and fitness. Despite the ubiquity of environmental variability, substantial knowledge gaps in our understanding of organismal responses to nonconstant thermal regimes remain. In the present study, using zebrafish (Danio rerio) as a model organism, we applied geometric morphometric methods to examine how challenging but ecologically realistic diel thermal fluctuations experienced during different life stages influence adult body shape, size, and condition. Zebrafish were exposed to either thermal fluctuations (22-32°C) or a static optimal temperature (27°C) sharing the same thermal mean during an early period spanning embryonic and larval ontogeny (days 0-30), a later period spanning juvenile and adult ontogeny (days 31-210), or a combination of both. We found that body shape, size, and condition were affected by thermal variability, but these plasticity-mediated changes were dependent on the timing of ontogenetic exposure. Notably, after experiencing fluctuating temperatures during early ontogeny, females displayed a deeper abdomen while males displayed an elongated caudal peduncle region. Moreover, males displayed beneficial acclimation of body condition under lifelong fluctuating temperature exposure, whereas females did not. The present study, using ecologically realistic thermal regimes, provides insight into the timing of environmental experiences that generate phenotypic variation in zebrafish.

Trans-oceanic genomic divergence of Atlantic cod ecotypes is associated with large inversions.

Chromosomal rearrangements such as inversions can play a crucial role in maintaining polymorphism underlying complex traits and contribute to the process of speciation. In Atlantic cod (Gadus morhua), inversions of several megabases have been identified that dominate genomic differentiation between migratory and nonmigratory ecotypes in the Northeast Atlantic. Here, we show that the same genomic regions display elevated divergence and contribute to ecotype divergence in the Northwest Atlantic as well. The occurrence of these inversions on both sides of the Atlantic Ocean reveals a common evolutionary origin, predating the >100 000-year-old trans-Atlantic separation of Atlantic cod. The long-term persistence of these inversions indicates that they are maintained by selection, possibly facilitated by coevolution of genes underlying complex traits. Our data suggest that migratory behaviour is derived from more stationary, ancestral ecotypes. Overall, we identify several large genomic regions-each containing hundreds of genes-likely involved in the maintenance of genomic divergence in Atlantic cod on both sides of the Atlantic Ocean.

Unintentional selection, unanticipated insights: introductions, stocking and the evolutionary ecology of fishes.

Natural environmental change has produced countless opportunities for species to disperse into and persist in habitats where they previously did not exist. Introduction and stocking programmes have facilitated similar sorts of colonization opportunities across considerably greater geographical scales and often in much shorter periods of time. Even though the mechanism of colonization differs, the result can be the same: evolutionary change in the colonizing population in response to novel selection pressures. As a consequence, some human-mediated fish transfers have unintentionally yielded novel research opportunities to study how phenotypes and genes interact with their environment and affect ecological and evolutionary change. The primary purpose here is to explore how work, directly or indirectly involved with human-mediated transfers, has unintentionally yielded novel research and research opportunities in fish ecology and evolution. Insights have produced new knowledge or altered previously held perceptions on topics such as local adaptation, rate of evolutionary change, phenotypic plasticity, alternative reproductive strategies, population structure and colonization probability. Well-documented stocking programmes, especially in terms of history, numbers and original population sources, can provide highly fertile ground for generating further insights on the ecology and evolution of fishes and of the factors likely to influence the success of conservation-based, restoration programmes.

Multigenerational hybridisation and its consequences for maternal effects in Atlantic salmon.

Outbreeding between segregating populations can be important from an evolutionary, conservation and economical-agricultural perspective. Whether and how outbreeding influences maternal effects in wild populations has rarely been studied, despite both the prominent maternal influence on early offspring survival and the known presence of fitness effects resulting from outbreeding in many taxa. We studied several traits during the yolk-feeding stage in multigenerational crosses between a wild and a domesticated Atlantic salmon (Salmo salar) population up to their third-generation hybrid in a common laboratory environment. Using cross-means analysis, we inferred that maternal additive outbreeding effects underlie most offspring traits but that yolk mass also underlies maternal dominant effects. As a consequence of the interplay between additive and dominant maternally controlled traits, offspring from first-generation hybrid mothers expressed an excessive proportion of residual yolk mass, relative to total mass, at the time of first feeding. Their residual yolk mass was 23-97% greater than those of other crosses and 31% more than that predicted by a purely additive model. Offspring additive, epistatic and epistatic offspring-by-maternal outbreeding effects appeared to further modify this largely maternally controlled cross-means pattern, resulting in an increase in offspring size with the percentage of domesticated alleles. Fitness implications remain elusive because of unknown phenotype-by-environment interactions. However, these results suggest how mechanistically co-adapted genetic maternal control on early offspring development can be disrupted by the effects of combining alleles from divergent populations. Complex outbreeding effects at both the maternal and offspring levels make the prediction of hybrid phenotypes difficult.

Old wine in new bottles: reaction norms in salmonid fishes.

Genetic variability in reaction norms reflects differences in the ability of individuals, populations and ultimately species to respond to environmental change. By increasing our understanding of how genotype × environment interactions influence evolution, studies of genetic variation in phenotypic plasticity serve to refine our capacity to predict how populations will respond to natural and anthropogenic environmental variability, including climate change. Given the extraordinary variability in morphology, behaviour and life history in salmonids, one might anticipate the research milieu on reaction norms in these fishes to be empirically rich and intellectually engaging. Here, I undertake a review of genetic variability in continuous and discontinuous (threshold) norms of reaction in salmonid fishes, as determined primarily (but not exclusively) by common-garden experiments. Although in its infancy from a numerical publication perspective, there is taxonomically broad evidence of genetic differentiation in continuous, threshold and bivariate reaction norms among individuals, families and populations (including inter-population hybrids and backcrosses) for traits as divergent as embryonic development, age and size at maturity, and gene expression. There is compelling inferential evidence that plasticity is heritable and that population differences in reaction norms can reflect adaptive responses, by natural selection, to local environments. As a stimulus for future work, a series of 20 research questions are identified that focus on reaction-norm variability, selection, costs and constraints, demographic and conservation consequences, and genetic markers and correlates of phenotypic plasticity.

Multiple paternity and variance in male fertilization success within Atlantic salmon Salmo salar redds in a naturally spawning population.

The incidence and magnitude of multiple paternity were estimated for a natural, unmanipulated spawning population of Atlantic salmon Salmo salar. Egg nests were surveyed in the autumn and sub-samples were excavated the following spring. Parentage data derived from microsatellite DNA revealed an unexpectedly high level of multiple paternity. Within a single redd, females may mate with as many as 16 different males, including small mature male parr and large anadromous males. Multiple paternity was most pronounced in areas of highest redd density, corresponding with increased abundances of mature male parr. In addition, there was considerable variation in success among males, although this variability did not depend upon the number of males participating in spawning. This work underscores the value of undertaking genetic studies on the mating systems of fishes in unmanipulated, natural environments.

Selective and genetic constraints on the evolution of body size in a stream-dwelling salmonid fish.

To examine constraints on evolution of larger body size in two stunted populations of brook charr (Salvelinus fontinalis) from a single river in Cape Race, Newfoundland, Canada, we measured viability selection acting on length-at-age traits, and estimated quantitative genetic parameters in situ (following reconstruction of pedigree information from microsatellite data). Furthermore we tested for phenotypic differentiation between the populations, and for association of high juvenile growth with early maturity that is predicted by life history theory. Within each population, selection differentials and estimates of heritabilities for length-at-age traits suggested that evolution of larger size is prevented by both selective and genetic constraints. Between the populations, phenotypic differentiation was found in length-at-age and age of maturation traits, whereas early maturation was associated with increased juvenile growth (relative to adult growth) both within and between populations. The results suggest an adaptive plastic response in age of maturation to juvenile growth rates that have a largely environmental basis of determination.

The influence of male parr body size and mate competition on fertilization success and effective population size in Atlantic salmon.

Alternative mating strategies in male Atlantic salmon, Salmo salar, are characterized by variability in body size and mate competition. Controlling breeding numbers of larger, older anadromous males, we examined whether body size of mature male parr influenced fertilization success and whether such an association was affected by mate competition among parr. Variation at three to four hypervariable microsatellite loci was used to determine individual paternity of 53-60 offspring from two or three nests from each experimental treatment. Although individual and total parr reproductive success differed significantly among nests within treatments, there was no relationship between parr size and individual reproductive success at any level of competition when anadromous males were involved. However, in a single treatment having no anadromous male, the influence of body size on parr fertilization success was highly significant. Combining data from all treatments, parr body size was an important predictor of the probability of an individual being involved in spawning. We found a negative relationship between total parr reproductive success and intensity of anadromous male competition. To our knowledge, the present study is the first to estimate the effective number of males from individual fertilization success in fish. Our estimates of Ne should not be taken as absolute and may have a downward bias because we did not sample all nests and we used a proxy for lifetime reproductive success. They do, however, illustrate how mature male parr can greatly increase the effective number of males when the latter is estimated from anadromous individuals alone. Although reproductive success by mature male parr increases the effective number of males, this increase seems likely to be most pronounced in natural populations when the number of anadromous males is low.

Collapse and recovery of marine fishes.

Overexploitation and subsequent collapse of marine fishes has focused attention on the ability of affected populations to recover to former abundance levels and on the degree to which their persistence is threatened by extinction. Although potential for recovery has been assessed indirectly, actual changes in population size following long-term declines have not been examined empirically. Here I show that there is very little evidence for rapid recovery from prolonged declines, in contrast to the perception that marine fishes are highly resilient to large population reductions. With the possible exception of herring and related species that mature early in life and are fished with highly selective equipment, my analysis of 90 stocks reveals that many gadids (for example, cod, haddock) and other non-clupeids (for example, flatfishes) have experienced little, if any, recovery as much as 15 years after 45-99% reductions in reproductive biomass. Although the effects of overfishing on single species may generally be reversible, the actual time required for recovery appears to be considerable. To exempt marine fishes from existing criteria used to assign extinction risk would be inconsistent with precautionary approaches to fisheries management and the conservation of marine biodiversity.

Population dynamics of exploited fish stocks at low population levels.

Models of population dynamics in which per capita reproductive success declines at low population levels (variously known as depensation, the Allee effect, and inverse density-dependence) predict that populations can have multiple equilibria and may suddenly shift from one equilibrium to another. If such depensatory dynamics exist, reduced mortality may be insufficient to allow recovery of a population after abundance has been severely reduced by harvesting. Estimates of spawner abundance and number of surviving progeny for 128 fish stocks indicated only 3 stocks with significant depensation. Estimates of the statistical power of the tests strengthen the conclusion that depensatory dynamics are not apparent for fish populations at the levels studied.

Mating success of alternative maturation phenotypes in male Atlantic salmon, Salmo salar.

Mature male parr successfully fertilized eggs of anadromous female Atlantic salmon, Salmo salar, in competition with anadromous males under simulated natural conditions. Mating situations were created in which mature male parr and anadromous males competing for the opportunity to spawn with an anadromous female differed in allelic forms of the same enzyme. Females deposited eggs into a sequence of 3 or 4 eggs nests. The mean proportion of eggs in a redd fertilized by parr increased with increasing numbers of parr present at a redd, reaching 23% at male parr: anadromous male ratios of 20:1. Single male parr fertilized, on average, 5% of the eggs in a redd. The proportion of eggs in an egg nest fertilized by parr also depended upon the order of egg nest construction, such that parr mating success was highest at the initial nest constructed and lowest at the final nest. Parr have relatively high fertilization success for their size when compared with the smaller maturation phenotype of other salmonids.