Lorenz Hauser

Molecular genetics and the stock concept in fisheries

The concept of a sustainable yield (SY, Gulland, 1983; Lannan et al., 1989) has dominated fisheries management for almost 50 years. The central idea is that each stock has a harvestable surplus, and that fisheries that do not exceed this will not compromise the stock’s natural perpetuation. A basic assumption is that the fishery targets a unit stock with definable patterns of recruitment and mortality. Although it is difficult to reach agreement on what constitutes a stock (Gauldie, 1991), the notion of population units with varying degrees of temporal or spatial integrity stimulated a quest to characterize and identify such assemblages. It became apparent that few species form single homogeneous populations, but rather that fish species are often composed of discrete stocks, and that these stocks may react to harvesting more or less independently. It was the idea of independent responses of different stocks to exploitation that demanded information on stock structure. Hence, the stock concept was linked strongly, at least in theory, with the desire to balance the impacts of harvesting with efforts to ensure continued economic returns. What was much more difficult to achieve than the theory was: (i) how to actually recognize a stock, and (ii) how to translate stock structure data into fishery practices.

Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus)

Although the effects of overfishing on species diversity and abundance are well documented, threats to the genetic diversity of marine fish populations have so far been largely neglected. Indeed, there seems to be little cause for concern, as even “collapsed” stocks usually consist of several million individuals, whereas population genetics theory suggests that only very small populations suffer significant loss of genetic diversity. On the other hand, in many marine species the genetically effective population size (Ne), which determines the genetic properties of a population, may be orders of magnitude smaller than the census population size (N). Here, microsatellite analyses of a time series of archived scales demonstrated a significant decline in genetic diversity in a New Zealand snapper population during its exploitation history. Effective population sizes estimated both from the decline in heterozygosity and from temporal fluctuations in allele frequency were five orders of magnitude smaller than census population sizes from fishery data. If such low Ne/N ratios are commonplace in marine species, many exploited marine fish stocks may be in danger of losing genetic variability, potentially resulting in reduced adaptability, population persistence, and productivity.

Single‐nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in nonmodel organisms

A supplemental issue on the topic of single-nucleotidepolymorphism-enabled (SNP) research in nonmodel organisms is especially timely. In this issue, organisms with reference genomes are considered to be ‘model’; ‘nonmodel’ organisms are those whose genomes are yet to be sequenced. Advances in DNA sequencing and SNP genotyping have provided profound insights into the genetics of model organisms, but until recently, studies of nonmodel species lagged behind because of the scarcity of sequence and markers (see Fig. 1). In the past year, Tautz et al. (2010) and associated papers in supplemental issue of Molecular Ecology described a revolutionary transition from studies of ‘molecular ecology’ to studies of ‘ecological genomics’. Concurrently, Allendorf et al. (2010) grappled with placing the new-found wealth of sequence and SNP information into a ‘conservation genomics’ context. This revolution in molecular genetics studies would have been difficult to forecast a few years ago. Molecular genetic studies provide exceptional insight into relationships, migration and evolution of natural populations (Morin et al. 2004). During the origins of molecular ecology, in the 1960s and 1970s, it became clear that techniques such as allozyme electrophoresis would provide a basic framework for understanding species interactions and adaptation and for conserving natural genetic variability (Utter et al. 1966, 1974; Avise et al. 1975). Technical limitations at the time restricted both the ability to explore the dynamics of genetic diversity in species exhibiting low levels of variation as well as the direct analysis of adaptive variation in the wild. During the following years, innovators began to dream of potential applications for conservation and management of economically exploited species that included using molecular markers to determine the population-of-origin of migrating animals (see papers in Ryman & Utter 1987; Waples & Aebersold 1990), an important focus of many papers in this issue. Recent decades were punctuated by improvements in molecular and statistical techniques that produced an array of tools relevant to ecological and evolutionary studies such as assignment tests, estimates of effective population size, fine-scale population structure, kinship analyses (e.g. Helyar et al. this issue; Waples & Waples this issue) and genome-wide surveys based upon an ever increasing resolution of individuals and populations. The advantages of genotyping polymorphic SNPs with high-throughput assays have created much interest (Vignal et al. 2002; Brumfield et al. 2003; Morin et al. 2004; Schlötterer 2004). Until recently, however, the scarcity of available DNA sequence data for nonmodel species limited marker development. Further, because of comparatively low mutation rates, cross-species amplification of primers for SNP analyses did not yield the same results as for microsatellites. For example, Miller et al. (2010) tested the OvineSNP50 BeadChip, developed for domestic sheep, in two related ungulates and found only about 1% of the nearly 50 000 SNP loci to be polymorphic. Therefore, the SNP assays or probes developed for one species were not likely to be useful in others, even though primers may cross-amplify. The current supplemental issue contains 22 papers that underline the advantages of SNPs, advocate the need for SNP research in nonmodel organisms, and chart advances in discovery and applications. Although progress is apparent across a broad array of taxa, most papers presented here focus upon species of fish. This outcome, beyond the bias of the workshop organizers, may be in part because of the well-developed multinational collaborations that coordinate the sharing of DNA Correspondence: J. E. Seeb, Fax: (206) 543 5728; E-mail: jseeb@uw.edu

Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots

Abstract To date, few studies have investigated the effects of inbreeding on sexually selected traits, although inbreeding depression on such traits can play an important role in the evolution and ecology of wild populations. Sexually selected traits such as ornamentation and courtship behaviour may not be primary fitness characters, but selection and dominance coefficients of their mutations will resemble those of traits under natural selection. Strong directional selection, for instance, through female mate‐choice, purges all but the most recessive deleterious mutations, and the remaining dominance variation will result in inbreeding depression once populations undergo bottlenecks. We analysed the effects of inbreeding on sexually selected traits (colour pattern and courtship behaviour) in the male guppy, Poecilia reticulata, from Trinidad, and found a significant decline in the frequency of mating behaviour and colour spots. Such effects occurred although the genetic basis of these traits, many of which are Y‐linked and hemizygous, would be expected to leave relatively little scope for inbreeding depression. Findings suggest that these sexually selected traits could reflect the genetic condition or health of males, and thus may be informative mate‐cue characters for female choice as suggested by the ‘good genes’ model.

An empirical comparison of SNPs and microsatellites for parentage and kinship assignment in a wild sockeye salmon (Oncorhynchus nerka) population.

Because of their high variability, microsatellites are still considered the marker of choice for studies on parentage and kinship in wild populations. Nevertheless, single nucleotide polymorphisms (SNPs) are becoming increasing popular in many areas of molecular ecology, owing to their high‐throughput, easy transferability between laboratories and low genotyping error. An ongoing discussion concerns the relative power of SNPs compared to microsatellites—that is, how many SNP loci are needed to replace a panel of microsatellites? Here, we evaluate the assignment power of 80 SNPs (HE = 0.30, 80 independent alleles) and 11 microsatellites (HE = 0.85, 192 independent alleles) in a wild population of about 400 sockeye salmon with two commonly used software packages (Cervus3, Colony2) and, for SNPs only, a newly developed software (SNPPIT). Assignment success was higher for SNPs than for microsatellites, especially for parent pairs, irrespective of the method used. Colony2 assigned a larger proportion of offspring to at least one parent than the other methods, although Cervus and SNPPIT detected more parent pairs. Identification of full‐sib groups without parental information from relatedness measures was possible using both marker systems, although explicit reconstruction of such groups in Colony2 was impossible for SNPs because of computation time. Our results confirm the applicability of SNPs for parentage analyses and refute the predictability of assignment success from the number of independent alleles.

An empirical verification of population assignment methods by marking and parentage data: hatchery and wild steelhead (Oncorhynchus mykiss) in Forks Creek, Washington, USA

Assignment tests are increasingly applied in ecology and conservation, although empirical comparisons of methods are still rare or are restricted to few of the available approaches. Furthermore, the performance of assignment tests in cases with low population differentiation, violations of Hardy–Weinberg equilibrium and unbalanced sampling designs has not been verified. The release of adult hatchery steelhead to spawn in Forks Creek in 1996 and 1997 provided an opportunity to compare the power of different assignment methods to distinguish their offspring from those of sympatric wild steelhead. We compared standard assignment methods requiring baseline samples (frequency, distance and Bayesian) and clustering approaches with and without baseline information, using six freely available computer programs. Assignments were verified by parentage data obtained for a subset of returning offspring. All methods provided similar assignment success, despite low differentiation between wild and hatchery fish (FST = 0.02). Bayesian approaches with baseline data performed best, whereas the results of clustering methods were variable and depended on the samples included in the analysis and the availability of baseline information. Removal of a locus with null alleles and equalizing sample sizes had little effect on assignments. Our results demonstrate the robustness of most assignment tests to low differentiation and violations of assumptions, as well as their utility for ecological studies that require correct classification of different groups.

ADVANCES IN THE MOLECULAR ANALYSIS OF FISH POPULATION STRUCTURE

Abstract The characteristics of high population and species biodiversity, taken together with the major anthropogenic threats arising from exploitation, introductions and habitat alterations, have ensured that fishes have received major attention from molecular biologists in the study of wild populations. Foremost among the various challenges has been the development of techniques to estimate population discreteness and associated patterns of dispersal and gene flow, so‐called stock structure analysis. Here, we review some recent developments in molecular technology, especially microsatellite analysis, and consider critically how such markers can be employed to estimate genetic differentiation in species exhibiting high mobility in open waters. Comparisons are made between microsatellites and other genetic markers (protein and DNA) in their ability to detect population structuring. Particular emphasis is placed on the need to design sampling programmes that take account of aspects of the biology of the sp...

Genetic isolation by distance and localized fjord population structure in Pacific cod (Gadus macrocephalus): limited effective dispersal in the northeastern Pacific Ocean

Genetic population structure of Pacific cod, Gadus macrocephalus, was examined across much of its northeast- ern Pacific range by screening variation at 11 microsatellite DNA loci. Estimates of FST (0.005 ± 0.002) and RST (0.010 ± 0.003) over all samples suggested that effective dispersal is limited among populations. Genetic divergence was highly cor- related with geographic distance in an isolation-by-distance (IBD) pattern along the entire coastal continuum in the north- eastern Pacific Ocean (~4000 km; r 2 = 0.83), extending from Washington State to the Aleutian Islands, and over smaller geographic distances for three locations in Alaska (~1700 km; r 2 = 0.56). Slopes of IBD regressions suggested average dis- persal distance between birth and reproduction of less than 30 km. Exceptions to this pattern were found in samples taken from fjord environments in the Georgia Basin (the Strait of Georgia (Canada) and Puget Sound (USA)), where populations were differentiated from coastal cod. Our results showed population structure at spatial scales relevant to fisheries manage- ment, both caused by limited dispersal along the coast and by sharp barriers to migration isolating smaller stocks in coastal fjord environments.

Fine-scale differentiation between sockeye salmon ecotypes and the effect of phenotype on straying.

A long-standing goal of evolutionary biology is to understand the factors that drive population divergence, local adaptation and speciation. In particular, the effect of selection against dispersers on gene flow and local adaptation has attracted interest, although empirical data on phenotypic characters of dispersers are scarce. Here, we used genetic and phenotypic data from beach and creek ecotypes of sockeye salmon (Oncorhynchus nerka) in Little Togiak Lake, Alaska, to examine the relationship between gene flow and phenotypic and genetic differentiation. Despite close geographic proximity, both genetic and phenotypic differentiation between beach and creek fish was high and significant in all sampling years, with beach males having deeper bodies than creek males. Strays, or fish that did not return to their natal sites to spawn as determined by genetic assignment, tended to morphologically resemble the fish in the population that they joined. Male strays from beaches to creeks were shallower bodied than other beach fish, and male strays from creeks to beaches were deeper bodied than other creek males. Our results indicated that selection against strays may be moderated by the strays’ phenotypic similarity to individuals in the recipient populations, but comparison of assignment results with long-term estimates of gene flow from FST still suggested that strays had low reproductive success.

Multiple ice‐age refugia in Pacific cod, Gadus macrocephalus

Pleistocene ice‐ages greatly influenced the historical abundances of Pacific cod, Gadus macrocephalus, in the North Pacific and its marginal seas. We surveyed genetic variation at 11 microsatellite loci and mitochondrial (mt) DNA in samples from twelve locations from the Sea of Japan to Washington State. Both microsatellite (mean H = 0.868) and mtDNA haplotype (mean h = 0.958) diversities were large and did not show any geographical trends. Genetic differentiation between samples was significantly correlated with geographical distance between samples for both microsatellites (FST = 0.028, r2 = 0.33) and mtDNA (FST = 0.027, r2 = 0.18). Both marker classes showed a strong genetic discontinuity between northwestern and northeastern Pacific populations that likely represents groups previously isolated during glaciations that are now in secondary contact. Significant differences appeared between samples from the Sea of Japan and Okhotsk Sea that may reflect ice‐age isolations in the northwest Pacific. In the northeast Pacific, a microsatellite and mtDNA partition was detected between coastal and Georgia Basin populations. The presence of two major coastal mtDNA lineages on either side of the Pacific Ocean basin implies at least two ice‐age refugia and separate postglacial population expansions facilitated by different glacial histories. Northward expansions into the Gulf of Alaska were possible 14–15 kyr ago, but deglaciation and colonization of the Georgia Basin probably occurred somewhat later. Population expansions were evident in mtDNA mismatch distributions and in Bayesian skyline plots of the three major lineages, but the start of expansions appeared to pre‐date the last glacial maximum.