Reproductive success in wild and hatchery male coho salmon.

Salmon produced by hatcheries have lower fitness in the wild than naturally produced salmon, but the factors underlying this difference remain an active area of research. We used genetic parentage analysis of alevins produced by experimentally mixed groups of wild and hatchery coho salmon (Oncorhynchus kisutch) to quantify male paternity in spawning hierarchies. We identify factors influencing paternity and revise previously published behavioural estimates of reproductive success for wild and hatchery males. We observed a strong effect of hierarchy size and hierarchy position on paternity: in two-male hierarchies, the first male sired 63% (±29%; s.d.) of the alevins and the second male 37% (±29%); in three-male hierarchies, the first male sired 64% (±26%), the second male 24% (±20%) and the third male 12% (±10%). As previously documented, hatchery males hold inferior positions in spawning hierarchies, but we also discovered that hatchery males had only 55-84% the paternity of wild males when occupying the same position within a spawning hierarchy. This paternity difference may result from inferior performance of hatchery males during sperm competition, female mate choice for wild males, or differential offspring survival. Regardless of its cause, the combination of inferior hierarchical position and inferior success at a position resulted in hatchery males having only half (51%) the reproductive success of wild males.

Global assessment of extinction risk to populations of Sockeye salmon Oncorhynchus nerka.

BACKGROUND: Concern about the decline of wild salmon has attracted the attention of the International Union for the Conservation of Nature (IUCN). The IUCN applies quantitative criteria to assess risk of extinction and publishes its results on the Red List of Threatened Species. However, the focus is on the species level and thus may fail to show the risk to populations. The IUCN has adapted their criteria to apply to populations but there exist few examples of this type of assessment. We assessed the status of sockeye salmon Oncorhynchus nerka as a model for application of the IUCN population-level assessments and to provide the first global assessment of the status of an anadromous Pacific salmon. METHODS/PRINCIPAL FINDINGS: We found from demographic data that the sockeye salmon species is not presently at risk of extinction. We identified 98 independent populations with varying levels of risk within the species' range. Of these, 5 (5%) are already extinct. We analyzed the risk for 62 out of 93 extant populations (67%) and found that 17 of these (27%) are at risk of extinction. The greatest number and concentration of extinct and threatened populations is in the southern part of the North American range, primarily due to overfishing, freshwater habitat loss, dams, hatcheries, and changing ocean conditions. CONCLUSIONS/SIGNIFICANCE: Although sockeye salmon are not at risk at the species-level, about one-third of the populations that we analyzed are at risk or already extinct. Without an understanding of risk to biodiversity at the level of populations, the biodiversity loss in salmon would be greatly underrepresented on the Red List. We urge government, conservation organizations, scientists and the public to recognize this limitation of the Red List. We also urge recognition that about one-third of sockeye salmon global population diversity is at risk of extinction or already extinct.

Priorities for improving the scientific foundation of conservation policy in North America.

The Society for Conservation Biology (SCB) can enhance conservation of biodiversity in North America by increasing its engagement in public policy. Toward this end, the North America Section of SCB is establishing partnerships with other professional organizations in order to speak more powerfully to decision makers and taking other actions--such as increasing interaction with chapters--geared to engage members more substantively in science-policy issues. Additionally, the section is developing a North American Biodiversity Blueprint, which spans the continental United States and Canada and is informed by natural and social science. This blueprint is intended to clarify the policy challenges for protecting continental biodiversity, to foster bilateral collaboration to resolve common problems, and to suggest rational alternative policies and practices that are more likely than current practices to sustain North America's natural heritage. Conservation scientists and practitioners can play a key role by drawing policy makers' attention to ultimate, as well as proximate, causes of biodiversity decline and to the ecological and economic consequences of not addressing these threats.

Elemental conservation units: communicating extinction risk without dictating targets for protection.

Conservation biologists mostly agree on the need to identify and protect biodiversity below the species level but have not yet resolved the best approach. We addressed 2 issues relevant to this debate. First, we distinguished between the abstract goal of preserving the maximum amount of unique biodiversity and the pragmatic goal of minimizing the loss of ecological goods and services given that further loss of biodiversity seems inevitable. Second, we distinguished between the scientific task of assessing extinction risk and the normative task of choosing targets for protection. We propose that scientific advice on extinction risk be given at the smallest meaningful scale: the elemental conservation unit (ECU). An ECU is a demographically isolated population whose probability of extinction over the time scale of interest (say 100 years) is not substantially affected by natural immigration from other populations. Within this time frame, the loss of an ECU would be irreversible without human intervention. Society's decision to protect an ECU ought to reflect human values that have social, economic, and political dimensions. Scientists can best inform this decision by providing advice about the probability that an ECU will be lost and the ecological and evolutionary consequences of that loss in a form that can be integrated into landscape planning. The ECU approach provides maximum flexibility to decision makers and ensures that the scientific task of assessing extinction risk informs, but remains distinct from, the normative social challenge of setting conservation targets.

Evolutionary consequences of fishing and their implications for salmon.

We review the evidence for fisheries-induced evolution in anadromous salmonids. Salmon are exposed to a variety of fishing gears and intensities as immature or maturing individuals. We evaluate the evidence that fishing is causing evolutionary changes to traits including body size, migration timing and age of maturation, and we discuss the implications for fisheries and conservation. Few studies have fully evaluated the ingredients of fisheries-induced evolution: selection intensity, genetic variability, correlation among traits under selection, and response to selection. Most studies are limited in their ability to separate genetic responses from phenotypic plasticity, and environmental change complicates interpretation. However, strong evidence for selection intensity and for genetic variability in salmon fitness traits indicates that fishing can cause detectable evolution within ten or fewer generations. Evolutionary issues are therefore meaningful considerations in salmon fishery management. Evolutionary biologists have rarely been involved in the development of salmon fishing policy, yet evolutionary biology is relevant to the long-term success of fisheries. Future management might consider fishing policy to (i) allow experimental testing of evolutionary responses to exploitation and (ii) improve the long-term sustainability of the fishery by mitigating unfavorable evolutionary responses to fishing. We provide suggestions for how this might be done.

Courtship and genetic quality: asymmetric males show their best side.

Fluctuating asymmetry (FA), the small random deviations from perfect morphological symmetry that result during development, is ubiquitous throughout the animal kingdom. In many species, FA seems to play a role in mate choice, perhaps because it signals an individual's genetic quality and health. However, the relationship between an individual's FA and behaviour is generally unknown: what do more asymmetric individuals do about their own asymmetry? We now show for the first time that individuals respond behaviourally to their own morphological FA in what appears to be an adaptive manner. During courtship, male guppies exhibiting high FA in ornamental colour, bias their displays towards their more colourful body side, thus potentially increasing their attractiveness by exaggerating the quantity of their orange signal. This appears to be a strictly behavioural male response to cues provided by females, as it does not occur when males court a non-reactive model female. Whether inferior males realize any mating advantage remains uncertain, but our study clearly demonstrates a behavioural response to random morphological asymmetries that appears to be adaptive. We propose that the tendency to show or otherwise use a 'best side' is common in nature, with implications for sexual signalling and the evolution of more pronounced asymmetries.

The evolution of parental care.

Our understanding of parental care behavior can be significantly advanced through the application of Williams's Principle, which states that reproduction has not only a benefit but also a cost to lifetime fitness. My laboratory has formalized Williams's Principle into the relative value theorem and found that its application to fishes, the taxa with the most diverse patterns of parental care, can help to explain which sex provides care and how much. In fishes, it is often the male that provides parental care, not because the male obtains greater benefits from this care, but probably because he pays fewer costs. Fish dynamically adjust their investment into parental care according to the number of offspring in their brood, past investment, genetic relatedness, and alternative mating opportunities, all of which affect the value of current offspring relative to potential future offspring. These results may also help us understand the joy and the challenges of parental care in humans.

BREEDING COMPETITION IN A PACIFIC SALMON (COHO: ONCORHYNCHUS KISUTCH): MEASURES OF NATURAL AND SEXUAL SELECTION.

In the breeding system of Pacific salmon, females compete for oviposition territories, and males compete to fertilize eggs. The natural selection in females and sexual selection in males likely has been responsible for their elaborate breeding morphologies and the dimorphism between the sexes. We quantified direct-selection intensities during breeding on mature coho salmon (Oncorhynchus kisutch), measured for seven phenotypic characters, including three secondary sexual characters. Wild and sea-ranched hatchery coho were used to enhance the range of phenotypes over which selection could be examined. The fish were allowed to breed in experimental arenas where we could quantify components of breeding success as well as estimate overall breeding success. We found that without competition, natural selection acts only on female body size for increased egg production; there is no detectable selection on males for the phenotypic distribution we used. Under competition, the opportunity for selection increased sixfold among females. Natural selection favored female body size and caudal-peduncle (tail) depth. Increased body size meant increased egg production and access to nesting territories. The caudal peduncle, used in burst swimming and nest digging, influenced both successful egg deposition and nest survival. Increasing density increased competition among females, though it did not significantly intensify natural selection on their characters. In males, competition increased the opportunity for selection 52-fold, which was nine times greater than for females. Sexual selection favored male body size and hooked snout length, both characters directly influencing male access to spawning opportunities. Selection on male body size was also affected significantly by breeding density. The ability of large males to control access to spawning females decreased at higher densities reflecting an increase in the operational sex ratio. Further, the relative success of small males, which could sneak access to spawning females, appeared to increase as that of intermediate-sized males decreased. Such disruptive selection may be responsible for the evolution of alternative reproductive tactics in salmon.

Breeding Success of Hatchery and Wild Coho Salmon (Oncorhynchus Kisutch) in Competition.

The divergence of hatchery fish in traits important for reproductive success has raised concerns about their ability to rehabilitate wild populations, and the threat that their inevitable straying poses to biological diversity through introgression. We therefore undertook a study of the breeding competition and success of sea-ranched hatchery fish placed in direct competition with wild fish. Experiments using wild and hatchery coho salmo (Oncorhynchus kisutch) were conducted within a controlled stream channel, allowing selective manipulation of breeding competition and density. Hatchery fish, particularly males, were competitively inferior to wild fish, being less aggressive and more submissive. As a consequence, hatchery males were denied access to ovipositing females; they partook in fewer spawnings, held more distal positions in spawning hierarchies, and attained only an estimated 62% of the breeding success of wild males. By contrast, competition did not appear to inhibit hatchery females as overtly as males. Hatchery and wild females exhibited similar levels of aggressive behavior, however hatchery females did suffer greater delays in the onset of breeding, failed to spawn larger proportions of their eggs, and lost more eggs to nest destruction by other females. They averaged an estimated 82% of the breeding success of wild females. There was thus a sex bias in the breeding disadvantage of hatchery fish, with males suffering more than females. Furthermore, the breeding disadvantage was density dependent with the relative success of hatchery to wild fish declining with increasing density. These results imply that hatchery fish have restricted abilities to rehabilitate wild populations, and may pose ecological and genetic threats to the conservation of wild populations.

NATURAL SELECTION RESULTING FROM FEMALE BREEDING COMPETITION IN A PACIFIC SALMON (COHO: ONCORHYNCHUS KISUTCH).

We studied breeding competition among wild female coho salmon (Oncorhynchus kisutch) and quantified natural selection acting on two important female characters: body size and kype size (a secondary sexual character used for fighting). We found that body size contributed to adult female fitness in three ways, through 1) an increased initial biomass of egg production, 2) the ability to acquire a high-quality territory for egg development, and 3) success in nest defense. These factors together resulted in as much as a 23-fold fitness advantage to the largest females in the population. The initial investment into egg production accounted for 50-60% of the measured intensity of natural selection on female body size. The effective investment into egg production (after female competition for territories) accounted for 40-50% of natural selection on female body size. Therefore, success in breeding competition is about as important as egg production in the current evolution of female body size. This is contrary to the expectation based on most fisheries literature. The size of a female's kype was also important to female reproductive success, although its contribution could not be separated from that of body size in our study. The strong natural selection that we have found for female competitive ability is presumably the basis for the evolution of female parental care in salmonids.

EVOLUTION OF ADULT FEMALE LIFE HISTORY AND MORPHOLOGY IN A PACIFIC SALMON (COHO: ONCORHYNCHUS KISUTCH).

Female competition on the spawning grounds can generate strong natural selection on female coho salmon (Oncorhynchus kisutch). We examined the morphology and investment into egg production of 13 wild and five hatchery populations. For each population, the degrees of breeding competition and migration arduousness were quantified. The results support the importance of breeding competition in the evolution of female morphology and life history. Female secondary sexual characters, including body coloration and length of kype (an extension of the upper jaw used for fighting), increase significantly with degree of breeding competition among populations. In contrast, egg size and female investment into egg production tend to decrease as competition increases, probably as a result of life-history trade-offs. The difficulty of migration to the spawning grounds also molds female morphology and life history. Salmon become more streamlined with increasing migration arduousness, and the biomass of eggs produced appears to decline. In hatcheries, where breeding competition is relaxed, characters associated with breeding competition and spawning performance are reduced. In contrast, egg size is increased. These results indicate that the morphology and life history of adult female salmon respond evolutionarily to local selection pressures, including both the biotic demands of breeding competition and the abiotic demands of migration.