Michael M. Hansen

Extent and scale of local adaptation in salmonid fishes: review and meta-analysis

What is the extent and scale of local adaptation (LA)? How quickly does LA arise? And what is its underlying molecular basis? Our review and meta-analysis on salmonid fishes estimates the frequency of LA to be ∼55–70%, with local populations having a 1.2 times average fitness advantage relative to foreign populations or to their performance in new environments. Salmonid LA is evident at a variety of spatial scales (for example, few km to>1000 km) and can manifest itself quickly (6–30 generations). As the geographic scale between populations increases, LA is generally more frequent and stronger. Yet the extent of LA in salmonids does not appear to differ from that in other assessed taxa. Moreover, the frequency with which foreign salmonid populations outperform local populations (∼23–35%) suggests that drift, gene flow and plasticity often limit or mediate LA. The relatively few studies based on candidate gene and genomewide analyses have identified footprints of selection at both small and large geographical scales, likely reflecting the specific functional properties of loci and the associated selection regimes (for example, local niche partitioning, pathogens, parasites, photoperiodicity and seasonal timing). The molecular basis of LA in salmonids is still largely unknown, but differential expression at the same few genes is implicated in the convergent evolution of certain phenotypes. Collectively, future research will benefit from an integration of classical and molecular approaches to understand: (i) species differences and how they originate, (ii) variation in adaptation across scales, life stages, population sizes and environmental gradients, and (iii) evolutionary responses to human activities.

Estimating the long‐term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples

Indigenous salmonid fish gene pools are affected by domesticated conspecifics, derived from aquaculture escapes and deliberate releases. Variability was examined at nine microsatellite loci in order to assess the long‐term impact of stocking domesticated trout in two brown trout populations. The study was based on analysis of two historical samples (1945–56), represented by old scale collections, and seven contemporary samples (1986–2000). In one population historical and contemporary samples were remarkably genetically similar despite more than a decade of intense stocking. Estimation of admixture proportions showed a small genetic contribution from domesticated trout (approximately 6%), and individual admixture analysis demonstrated a majority of nonadmixed individuals. The expected genetic contribution by domesticated trout was 64%, assessed from the number of stocked trout and assuming equal survival and reproductive performance of wild and domesticated trout. This demonstrates poor performance and low fitness of domesticated trout in the wild. In another population there was a strong genetic contribution from domesticated trout (between 57% and 88% in different samples), both in samples from a broodstock thought to represent the indigenous population and in a sample of wild spawners. Survival of domesticated trout and admixture with indigenous fish in the broodstock and subsequent stocking into the river, combined with a low population size of native trout relative to the number of stocked trout, could explain the observed introgression. Few nonadmixed individuals remained in the introgressed population, and I discuss how individual admixture analysis can be used to identify and conserve nonintrogressed remains of the population.

Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis

The study of hybrid zones is central to our understanding of the genetic basis of reproductive isolation and speciation, yet very little is known about the extent and significance of hybrid zones in marine fishes. We examined the population structure of cod in the transition area between the North Sea and the Baltic Sea employing nine microsatellite loci. Genetic differentiation between the North Sea sample and the rest increased along a transect to the Baltic proper, with a large increase in level of differentiation occurring in the Western Baltic area. Our objective was to determine whether this pattern was caused purely by varying degrees of mechanical mixing of North Sea and Baltic Sea cod or by interbreeding and formation of a hybrid swarm. Simulation studies revealed that traditional Hardy–Weinberg analysis did not have sufficient power for detection of a Wahlund effect. However, using a model‐based clustering method for individual admixture analysis, we were able to demonstrate the existence of intermediate genotypes in all samples from the transition area. Accordingly, our data were explained best by a model of a hybrid swarm flanked by pure nonadmixed populations in the North Sea and the Baltic Sea proper. Significant correlation of gene identities across loci (gametic phase disequilibrium) was found only in a sample from the Western Baltic, suggesting this area as the centre of the apparent hybrid zone. A hybrid zone for cod in the ecotone between the high‐saline North Sea and the low‐saline Baltic Sea is discussed in relation to its possible origin and maintenance, and in relation to a classical study of haemoglobin variation in cod from the Baltic Sea/Danish Belt Sea, suggesting mixing of two divergent populations without interbreeding.

Oceanic Spawning Migration of the European Eel (Anguilla anguilla)

Satellite tracking technology has allowed scientists to map part of the migration route of the European eel. European eels (Anguilla anguilla) undertake a ~5000-kilometer (km) spawning migration from Europe to the Sargasso Sea. The larvae are transported back to European waters by the Gulf Stream and North Atlantic Drift. However, details of the spawning migration remain unknown because tracking eels in the Atlantic Ocean has, so far, eluded study. Recent advances in satellite tracking enable investigation of migratory behavior of large ocean-dwelling animals. However, sizes of available tags have precluded tracking smaller animals like European eels. Here, we present information about the swimming direction, depth, and migratory behavior of European eels during spawning migration, based on a miniaturized pop-up satellite archival transmitter. Although the tagging experiment fell short of revealing the full migration to the Sargasso Sea, the data covered the first 1300 km and provided unique insights.

Marine landscapes and population genetic structure of herring (Clupea harengus L.) in the Baltic Sea.

Numerically small but statistically significant genetic differentiation has been found in many marine fish species despite very large census population sizes and absence of obvious barriers to migrating individuals. Analyses of morphological traits have previously identified local spawning groups of herring (Clupea harengus L.) in the environmentally heterogeneous Baltic Sea, whereas allozyme markers have not revealed differentiation. We analysed variation at nine microsatellite loci in 24 samples of spring‐spawning herring collected at 11 spawning locations throughout the Baltic Sea. Significant temporal differentiation was observed at two locations, which we ascribe to sympatrically spawning but genetically divergent ‘spawning waves’. Significant differentiation was also present on a geographical scale, though pairwise FST values were generally low, not exceeding 0.027. Partial Mantel tests showed no isolation by geographical distance, but significant associations were observed between genetic differentiation and environmental parameters (salinity and surface temperature) (0.001 < P≤ 0.099), though these outcomes were driven mainly by populations in the southwestern Baltic Sea, which also exhibits the steepest environmental gradients. Application of a novel method for detecting barriers to gene flow by combining geographical coordinates and genetic differentiation allowed us to identify two zones of lowered gene flow. These zones were concordant with the separation of the Baltic Sea into major basins, with environmental gradients and with differences in migration behaviour. We suggest that similar use of landscape genetics approaches may increase the understanding of the biological significance of genetic differentiation in other marine fishes.

The problem of sampling families rather than populations: Relatedness among individuals in samples of juvenile brown trout Salmo trutta L

In species exhibiting a nonrandom distribution of closely related individuals, sampling of a few families may lead to biased estimates of allele frequencies in populations. This problem was studied in two brown trout populations, based on analysis of mtDNA and microsatellites. In both samples mtDNA haplotype frequencies differed significantly between age classes, and in one sample 17 out of 18 individuals less than 1 year of age shared one particular mtDNA haplotype. Estimates of relatedness showed that these individuals most likely represented only three full‐sib families. Older trout exhibiting the same haplotypes generally were not closely related.

Analysis of microsatellite DNA from old scale samples of Atlantic salmon Salmo salar: a comparison of genetic composition over 60 years

Microsatellite analysis was applied to scale samples of Atlantic salmon collected up to 60 years ago. Samples from the 1930s, from a now endangered Danish population, were compared with recent samples (1989), to test if the present population consists of descendants from the original one. Allele frequencies had changed over time, but individuals from the two samples caught about 60 years apart clustered together when compared with the closest neighbouring population and another reference population. However, fewer alleles were detected in the recent sample from the endangered population, most likely due to a population bottleneck or sampling artefacts.

Monitoring adaptive genetic responses to environmental change

Widespread environmental changes including climate change, selective harvesting and landscape alterations now greatly affect selection regimes for most organisms. How animals and plants can adapt to these altered environments via contemporary evolution is thus of strong interest. We discuss how to use genetic monitoring to study adaptive responses via repeated analysis of the same populations over time, distinguishing between phenotypic and molecular genetics approaches. After describing monitoring designs, we develop explicit criteria for demonstrating adaptive responses, which include testing for selection and establishing clear links between genetic and environmental change. We then review a few exemplary studies that explore adaptive responses to climate change in Drosophila, selective responses to hunting and fishing, and contemporary evolution in Daphnia using resurrected resting eggs. We further review a broader set of 44 studies to assess how well they meet the proposed criteria, and conclude that only 23% fulfill all criteria. Approximately half (43%) of these studies failed to rule out the alternative hypothesis of replacement by a different, better‐adapted population. Likewise, 34% of the studies based on phenotypic variation did not test for selection as opposed to drift. These shortcomings can be addressed via improved experimental designs and statistical testing. We foresee monitoring of adaptive responses as a future valuable tool in conservation biology, for identifying populations unable to evolve at sufficiently high rates and for identifying possible donor populations for genetic rescue. Technological advances will further augment the realization of this potential, especially next‐generation sequencing technologies that allow for monitoring at the level of whole genomes.

Long-term effective population sizes, temporal stability of genetic composition and potential for local adaptation in anadromous brown trout ( Salmo trutta ) populations

We examined the long‐term temporal (1910s to 1990s) genetic variation at eight microsatellite DNA loci in brown trout (Salmo trutta L) collected from five anadromous populations in Denmark to assess the long‐term stability of genetic composition and to estimate effective population sizes (Ne). Contemporary and historical samples consisted of tissue and archived scales, respectively. Pairwise θST estimates, a hierarchical analysis of molecular variance (amova) and multidimensional scaling analysis of pairwise genetic distances between samples revealed much closer genetic relationships among temporal samples from the same populations than among samples from different populations. Estimates of Ne, using a likelihood‐based implementation of the temporal method, revealed Ne ≥ 500 in two of three populations for which we have historical data. A third population in a small (3 km) river showed Ne ≥ 300. Assuming a stepping‐stone model of gene flow we considered the relative roles of gene flow, random genetic drift and selection to assess the possibilities for local adaptation. The requirements for local adaptation were fulfilled, but only adaptations resulting from strong selection were expected to occur at the level of individual populations. Adaptations resulting from weak selection were more likely to occur on a regional basis, i.e. encompassing several populations. Ne appears to have declined recently in at least one of the studied populations, and the documented recent declines of many other anadromous brown trout populations may affect the persistence of local adaptation.

GENETIC VARIATION IN TIME AND SPACE: MICROSATELLITE ANALYSIS OF EXTINCT AND EXTANT POPULATIONS OF ATLANTIC SALMON

Information on genetic composition of past and present populations may be obtained by analyzing DNA from archival samples. A study is presented on the genetic population structure of extant and extinct local populations of Atlantic salmon from 1913 to 1989 using dried scales as a source of DNA. Variation at six microsatellite loci was studied. Tests for differentiation among populations and among time series within populations showed that population structure was stable over time. This was also confirmed by a neighbor‐joining dendrogram, which showed a clear clustering of samples from individual rivers that covered a time span of up to 76 years. These results suggest that salmon populations evolve as semi‐independent units connected by modest amounts of gene flow. Additionally, a clear association between geographic and genetic distance was found. This relationship has otherwise been difficult to establish in several recent studies. The discrepancy may be due to impact of human activities on the genetic structure of present populations, whereas old samples represent populations in a more unaffected state. However, other explanations related to differences in the sampling of past and present populations may be equally valid.