Julian J. Dodson

Phylogeographic structure in mitochondrial DNA of the lake whitefish (Coregonus clupeaformis) and its relation to Pleistocene glaciations

Restriction‐fragment length polymorphisms were employed to evaluate the phylogenetic relationships, the genetic diversity and the geographic structure in mitochondrial DNA (mtDNA) lineages of the lake whitefish, Coregonus clupeaformis. Thirteen restriction enzymes that produced 148 restriction fragments were used to assay mtDNAs of 525 specimens collected among 41 populations. The sampling covered the entire range of the species, from Alaska to Labrador. Four distinct phylogeographic assemblages were identified. The Beringian assemblage, confined to Yukon and Alaska, was phylogenetically distinct from other assemblages and exhibited the highest level of nucleotide diversity. The Acadian assemblage was confined to southeastern North America and composed of a unique mtDNA clade. The Atlantic assemblage was confined to southern Québec and the northeastern United States and was also observed among anadromous populations of northern Hudson Bay. This group was highly polymorphic and responsible for most of the mtDNA diversity observed outside Beringia. The Mississippian assemblage occupied most of the actual range of lake whitefish, from the Mackenzie delta to Labrador. Ninety‐two percent of all whitefish of this proposed origin belonged to a single mtDNA haplotype. Overall, the diversity, the geographic structure and the times of divergence of mtDNA phylogenetic assemblages correlate with the Pleistocene glaciations classically assumed to have dramatically altered the genetic diversity of northern fishes in recent evolutionary times. Our results emphasize the dominant role of these catastrophic events in shaping the population genetic structure of lake whitefish.

Allopatric origin of sympatric populations of lake whitefish (Coregonus clupeaformis) as revealed by mitochondrial-DNA restriction analysis

In the paper, restriction-fragment length polymorphisms in mitochondrial DNA (mtDNA) were studied to test the hypothesis that sympatric populations of lake whitefish in the Allegash basin have recently diverged through sympatric speciation. Thirteen restriction enzymes were used to analyze mtDNA of 156 specimens representing 13 populations from eastern Canada and northern Maine where normal and dwarf phenotypes of whitefish exist in sympatry and allopatry. Two monophyletic assemblages of populations that exhibit different geographic distributions were iden- tified. One showed an eastern distribution that expands from Cape Breton to the Allegash basin and the other exhibits a more western distribution. The Allegash basin was the only area of overlap. The western assemblage exhibited the normal size phenotype in all cases, whereas the eastern assemblage exhibited the normal size phenotype in allopatric conditions and the dwarf size phe- notype in sympatry. The existence of sympatric pairs in the Allegash basin result from the secondary contact of two monophyletic groups of whitefish that evolved allopatrically in separate refugia during the last glaciation events. The weak mtDNA difference of sympatric pairs suggests that speciation of lake whitefish in eastern North America was accompanied by only minor alterations of the ancestral gene pool.

Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation

Disentangling evolutionary forces that may interact to determine the patterns of genetic differentiation within and among wild populations is a major challenge in evolutionary biology. The objective of this study was to assess the genetic structure and the potential influence of several ecological variables on the extent of genetic differentiation at multiple spatial scales in a widely distributed species, the Atlantic salmon, Salmo salar. A total of 2775 anadromous fish were sampled from 51 rivers along the North American Atlantic coast and were genotyped using 13 microsatellites. A Bayesian analysis clustered these populations into seven genetically and geographically distinct groups, characterized by different environmental and ecological factors, mainly temperature. These groups were also characterized by different extent of genetic differentiation among populations. Dispersal was relatively high and of the same magnitude within compared to among regional groups, which contrasted with the maintenance of a regional genetic structure. However, genetic differentiation was lower among populations exchanging similar rates of local as opposed to inter‐regional migrants, over the same geographical scale. This raised the hypothesis that gene flow could be constrained by local adaptation at the regional scale. Both coastal distance and temperature regime were found to influence the observed genetic structure according to landscape genetic analyses. The influence of other factors such as latitude, river length and altitude, migration tactic, and stocking was not significant at any spatial scale. Overall, these results suggested that the interaction between gene flow and thermal regime adaptation mainly explained the hierarchical genetic structure observed among Atlantic salmon populations.

Ecological determinants and temporal stability of the within‐river population structure in Atlantic salmon (Salmo salar L.)

A gene diversity analysis was performed using microsatellite loci in order to (i) describe the extent and pattern of population structure in Atlantic salmon (Salmo salar L.) within a river system; (ii) establish the importance of quantifying the signal:noise ratio in accurately estimating population structure; and (iii) assess the potential usefulness of two evolutionary models in explaining within‐river population structure from the ecological and habitat characteristics of Atlantic salmon. We found weak, yet highly significant microscale spatial patterning after accounting for variance among temporal replicates within sites. Lower genetic distances were observed among temporal samples at four sampling sites whereas no evidence for temporal stability was observed at the other three locations. The component of genetic variance attributable to either temporal instability and/or random sampling errors was almost three times more important than the pure spatial component. This indicates that not considering signal:noise ratio may lead to an important overestimation of genetic substructuring in situations of weak genetic differentiation. This study also illustrates the usefulness of the member–vagrant hypothesis to generate a priori predictions regarding the number of subpopulations that should compose a species, given its life‐history characteristics and habitat structure. On the other hand, a metapopulation model appears better suited to explain the extent of genetic divergence among subpopulations, as well as its temporal persistence, given the reality of habitat patchiness and environment instability. We thus conclude that the combined use of both models may offer a promising avenue for studies aiming to understand the dynamics of genetic structure of species found in unstable environments.

CLINAL VARIATION IN MHC DIVERSITY WITH TEMPERATURE: EVIDENCE FOR THE ROLE OF HOST–PATHOGEN INTERACTION ON LOCAL ADAPTATION IN ATLANTIC SALMON

Abstract In vertebrates, variability at genes of the Major Histocompatibility Complex (MHC) represents an important adaptation for pathogen resistance, whereby high allelic diversity confers resistance to a greater number of pathogens. Pathogens can maintain diversifying selection pressure on their hosts immune system that can vary in intensity based on pathogen richness, pathogen virulence, and length of the cohabitation period, which tend to increase with temperature. In this study, we tested the hypothesis that genetic diversity of MHC increases with temperature along a latitudinal gradient in response to pathogen selective pressure in the wild. A total of 1549 Atlantic salmon from 34 rivers were sampled between 46°N and 58°N in Eastern Canada. The results supported our working hypothesis. In contrast to the overall pattern observed at microsatellites, MHC class II allelic diversity increased with temperature, thus creating a latitudinal gradient. The observed temperature gradient was more pronounced for MHC amino acids of the peptide-binding region (PBR), a region that specifically binds to pathogens, than for the non-PBR. For the subset of rivers analyzed for bacterial diversity, MHC amino acid diversity of the PBR also increased significantly with bacterial diversity in each river. A comparison of the relative influence of temperature and bacterial diversity revealed that the latter could have a predominant role on MHC PBR variability. However, temperature was also identified as an important selective agent maintaining MHC diversity in the wild. Based on the bacteria results and given the putative role of temperature in shaping large-scale patterns of pathogen diversity and virulence, bacterial diversity is a plausible selection mechanism explaining the observed association between temperature and MHC variability. Therefore, we propose that genetic diversity at MHC class II represents local adaptation to cope with pathogen diversity in rivers associated with different thermal regimes. This study illuminates the link between selection pressure from the environment, host immune adaptation, and the large-scale genetic population structure for a nonmodel vertebrate in the wild.

GENETIC EVIDENCE FOR REPRODUCTIVE ISOLATION AND MULTIPLE ORIGINS OF SYMPATRIC TROPHIC ECOTYPES OF WHITEFISH (COREGONUS)

We assessed variation in mitochondrial DNA (mtDNA) by restriction fragment length polymorphism (RFLP) analysis and in nuclear genes by allozyme analysis among sympatric pairs of limnetic and benthic ecotypes of whitefish (Coregonus) coexisting in three lakes of southern Yukon to address three evolutionary questions regarding their origins. Are sympatric low and high gill‐raker count ecotypes genetically differentiated? Are they issued from monophyletic or polyphyletic evolutionary events? If they are polyphyletic in origins, did they originate from multiple allopatric speciation events or intralacustrine radiation? Our results corroborated previous genetic and ecological studies of these ecotypes, indicating that they represent genetically distinct reproductive units, and therefore refuting the hypothesis of phenotypic polymorphism within a single population. However, the amount of gene flow between ecotypes varied among lakes, correlating with the extent of morphological differentiation and the potential for premating reproductive isolation. The results indicated a polyphyletic origin of ecotypes whereby each of them have been expressed independently more than once. In the two lakes of Squanga Creek drainage, the existence of sympatric pairs was best explained by the secondary contact of two monophyletic whitefish groups that evolved in allopatry during the last glaciation events. In Dezadeash L. of Alsek R. drainage, our results could not verify either sympatric or allopatric (or microallopatric) origin of ecotypes. Regardless of the mode of speciation involved in their origins, these sympatric whitefish populations provided further evidence that Pleistocene glaciation events created conditions favoring rapid divergence and phenotypic differentiation among northern freshwater fishes.

DIFFERENTIAL REPRODUCTIVE SUCCESS AND HERITABILITY OF ALTERNATIVE REPRODUCTIVE TACTICS IN WILD ATLANTIC SALMON (SALMO SALAR L.)

Abstract A critical step in understanding the evolution and maintenance of alternative reproductive tactics is to obtain accurate comparisons of their fitness and to determine factors influencing individual status. In this study, we first used individual multilocus genotypic information to compare reproductive success between two alternative reproductive tactics of anadromous Atlantic salmon (Salmo salar L.) in their natural environments. We also documented the effects of the quality of the rearing environment and of paternal reproductive tactics on heritability of juvenile growth, which is an important component of individual status. Results showed that large dominant salmon (multisea winter) had higher reproductive success than smaller satellite individuals (grilse). Also, there was a status difference associated with both habitat and male tactic. Overall, offspring produced in streams were bigger than those produced in the main river stretch. Grilse also produced bigger offspring than those fathered by multisea winter males. Heritability of juvenile growth was significant but varied according to quality of habitat: higher heritability estimates were observed in higher quality habitats (streams) than in lower quality habitats (main river stretch). Heritability estimates for juvenile growth varied as well, depending on male tactic, with progeny fathered by multisea winter males having higher values than those fathered by grilse. Together, these results indicate that a combination of additive genetic effects, parental life history and habitat quality will ultimately shape juvenile growth rate, which is the main determinant of status and of subsequent choice of life‐history tactics.

The nature and role of learning in the orientation and migratory behavior of fishes

SynopsisFish migration may be viewed as the product of two processes; the selection and tracking of optimal environmental conditions through time and space, and the use of predictive information about environmental structure to bias movements towards a goal. The establishment and maintenance of directional bias is based on the interaction of experience and instinct. The preoccupation of much fish orientation research with innate fixed patterns of behavior on one hand and hydrodynamics on the other has led us to underestimate the possibility that orientation is a flexible process relying on developmental sequences, calibration of the motor-sensory interaction based on experience and the learning of environmental pattern. Evidence illustrating how experience and learning may influence the direction of movement and how the goal is recognized is presented according to two general categories: (a) imprinting and early experience and (b), spatial learning, including the social transmission of migratory routes and directions. In the first category, the olfactory hypothesis of salmon homing is briefly reviewed and new data presented describing olfactory imprinting in Atlantic salmon,Salmo salar. In the second category, evidence is presented demonstrating the modifiability of sun-compass orientation and the ability of some fish species to learn the spatial distribution of landmarks. The role of social transmission in the migration of coral reef fishes is reviewed. The possible role of these learning phenomena in the formation of familiar area maps, route-based and location-based navigation and the critical distance factor is considered. The relationship between life history and the nature of learning in migratory orientation is discussed

Living with uncertainty: genetic imprints of climate shifts in East Pacific anchovy ( Engraulis mordax ) and sardine ( Sardinops sagax )

In the upwelling zone of the northeastern Pacific, cold nutrient‐rich conditions alternate with warm nutrient‐poor intervals on timescales ranging from months to millennia. In this setting, the abundances of Pacific sardine (Sardinops sagax) and northern anchovy (Engraulis mordax) fluctuate by several orders of magnitude, with sardine dominating during warm conditions and anchovy dominating during cool conditions. Two population models can explain the response of these fishes to adverse conditions. Under the basin model, species distributions contract to a central (optimal) range during population crashes. Expectations of this model may include a single range‐wide population with a decline in genetic diversity on both sides of a central refuge. In contrast, the self‐recruitment model invokes a series of local oceanographic domains that maintain semi‐isolated subpopulations. During adverse conditions, some subpopulations cannot complete the life cycle within the local environment and are extirpated. Expectations of this model include some degree of population genetic structure and no clear gradient in genetic diversity. We examined mitochondrial DNA cytochrome b sequences to assess these competing models for anchovy (N = 196; 539 bp) and sardine (N = 107; 425 bp). The mitochondrial DNA gene genealogies are shallow but diverse for both species. Haplotype frequencies are homogeneous among subpopulations, but genetic diversities peak for both species along Baja California and adjacent southern California. Mismatch distributions and Tajimas D‐values reveal distinctive signatures of population bottlenecks and expansions. Sardine haplotypes coalesce at ~241 000 years bp, with an initial female effective population size Nf0 = 0 followed by exponential growth to Nf1 = 115 million. Anchovy haplotypes coalesce at ~282 000 years bp, with an initial population size of Nf0 = 14 000, followed by exponential growth to Nf1 = 2.3 million. These results indicate a founder event for sardine and a severe population decline for anchovy in the California Current during the late Pleistocene. Overall, these data support the basin model on decadal timescales, although local recruitment may dominate on shorter timescales.

INFLUENCE OF INDIVIDUAL BODY SIZE AND VARIABLE THRESHOLDS ON THE INCIDENCE OF A SNEAKER MALE REPRODUCTIVE TACTIC IN ATLANTIC SALMON

Abstract In the conditional strategy model, divergence in reproductive phenotypes depends on whether the individuals condition is above or below a genetically determined threshold. The relative contribution of the genetic and environmental components that lead to the expression of a reproductive tactic by an individual is not well understood. In the present field study, we determined when condition diverged between males that develop the mature parr phenotype and those that do not in Atlantic salmon (Salmo salar). We also investigated the uniformity of the threshold value in the population. We sampled mature parr and immature males at age one, of the same population at six different sites for four consecutive years. Our study provides an example of the interaction of genotype and environment on the expression of a reproductive tactic. Size was significantly greater for future mature parr than for future immature males as early as 20 days after hatching (emergence), suggesting that there may be a parental effect component in the tactic adopted, since no exogenous feeding takes place before this time. Size advantage at emergence was maintained through the next spring at age one to different degrees depending on the year, thus suggesting the presence of an environmental component of tactic expression. Our results support the contention that within the conditional strategy, the environment faced by a male and his condition at the moment of reproduction consistently predicts neither the environment faced by his offspring nor the fitness they will obtain by expressing the same tactic as their father. Furthermore, higher mean size at a site did not always translate into a higher proportion of mature parr, therefore supporting the hypothesis that thresholds vary across habitats within the same population.