Pacific Salmon, Oncorhynchus spp., and the Definition of "Species" Under the Endangered Species Act

For purposes ofthe Endangered Species Act (ESA), a "species" is defined to include "any distinct population segment of any species of vertebrate fish or wildlife which interbreeds when mature. "Federal agencies charged with carrying out the provisions of the ESA have struggled for over a decade to develop a consistent approach for interpreting the term "distinct population segment." This paper outlines such an approach and explains in some detail how it can be applied to ESA evaluations of anadromous Pacific salmonids. The following definition is proposed: A population (or group of populations) will be considered "distinct" (and hence a "species ")for purposes of the ESA if it represents an evolutionarily significant unit (ESU) of the biological species. A population must satisfy two criteria to be considered an ESU: 1) It must be substantially reproductively isolated from other conspecific population units, and 2) It must represent an important component in the evolutionary legacy of the species. Isolation does not have to be absolute, but it must be strong enough to permit evolutionarily important differences to accrue in different population units. The second criterion would be met if the population contributes substantially to the ecological/genetic diversity of the species as a whole. Insights into the extent of reproductive isolation can be provided by movements of tagged fish, natural recolonization rates observed in other populations, measurements of genetic differences between populations, and evaluations of the efficacy of natural barriers. Each of these methods has its limitations. Identification of physical barriers to genetic exchange can help define the geographic extent of distinct populations, but reliance on physical features alone can be misleading in the absence of supporting biological information. Physical tags provide information about the movements of individual fish but not the genetic consequences of migration. Furthermore, measurements ofc urrent straying or recolonization rates provide no direct information about the magnitude or consistency of such rates in the past. In this respect, data from protein electrophoresis or DNA analyses can be very useful because they reflect levels of gene flow that have occurred over evolutionary time scales. The best strategy is to use all available lines of evidence for or against reproductive isolation, recognizing the limitations of each and taking advantage of the often complementary nature of the different types of information. If available evidence indicates significant reproductive isolation, the next step is to determine whether the population in question is of substantial ecological/genetic importance to the species as a whole. In other words, if the population became extinct, would this event represent a significant loss to the ecological/genetic diversity of thes pecies? In making this determination, the following questions are relevant: 1) Is the population genetically distinct from other conspecific populations? 2) Does the population occupy unusual or distinctive habitat? 3) Does the population show evidence of unusual or distinctive adaptation to its environment? Several types of information are useful in addressing these questions. Again, the strengths and limitations of each should be kept in mind in making the evaluation. Phenotypic/life-history traits such as size, fecundity, and age and time of spawning may reflect local adaptations of evolutionary importance, but interpretation of these traits is complicated by their sensitivity to environmental conditions. Data from protein electrophoresis or DNA analyses provide valuable insight into theprocessofgenetic differentiation among populations but little direct information regarding the extent of adaptive genetic differences. Habitat differences suggest the possibility for local adaptations but do not prove that such adaptations exist. The framework suggested here provides a focal point for accomplishing the majorgoal of the Act-to conserve the genetic diversity of species and the ecosystems they inhabit. At the same time, it allows discretion in the listing of populations by requiring that they represent units of real evolutionary significance to the species. Further, this framework provides a means of addressing several issues of particular concern for Pacific salmon, including anadromous/nonanadromous population segments, differences in run-timing, groups of populations, introduced populations, and the role of hatchery fish

Seed Banks, Salmon, and Sleeping Genes: Effective Population Size in Semelparous, Age-Structured Species with Fluctuating Abundance

Previous studies reached contrasting conclusions regarding how fluctuations in abundance affect Ne in semelparous species with variable age at maturity: that Ne is determined by the arithmetic mean N among the T years within a generation (Ne ≈ T͞͞N̅͞t; monocarpic plants with seed banks) or the harmonic mean t (N ≈ TÑ ; Pacific salmon). I show that these conclusions arise from different model assumptions rather than inherent differences between the species. Sequentially applying standard, discrete-generation formulas for inbreeding Ne to a series of nominal generations accurately predicts the multigenerational rate of increase in inbreeding. Variability in mean realized reproductive success across years (k̅t) is the most important factor determining Ne and Ne/N. When abundance is driven by random variation in k̅t, Ne≤ TÑt\u3c TN̅ . With random variation in Nt and constant per capita seed production (C), variation in k̅t is low and Ne ~ TÑt; however, if C varies among years, Ne can be closer to TÑt. Because population regulation affects the genetic contribution of entire cohorts of monocarpic perennials, Ne for these species may be more closely approximated by TÑt than by TN̅ .With density-dependent compensation, and Cov (kt, Nt) \u3c 0 is further reduced because relatively few breeders make a disproportionate contribution to the next generation

Seed Banks, Salmon, and Sleeping Genes: Effective Population Size in Semelparous, Age-Structured Species with Fluctuating Abundance

Previous studies reached contrasting conclusions regarding how fluctuations in abundance affect Ne in semelparous species with variable age at maturity: that Ne is determined by the arithmetic mean N among the T years within a generation (Ne ≈ T͞͞N̅͞t; monocarpic plants with seed banks) or the harmonic mean t (N ≈ TÑ ; Pacific salmon). I show that these conclusions arise from different model assumptions rather than inherent differences between the species. Sequentially applying standard, discrete-generation formulas for inbreeding Ne to a series of nominal generations accurately predicts the multigenerational rate of increase in inbreeding. Variability in mean realized reproductive success across years (k̅t) is the most important factor determining Ne and Ne/N. When abundance is driven by random variation in k̅t, Ne≤ TÑt\u3c TN̅ . With random variation in Nt and constant per capita seed production (C), variation in k̅t is low and Ne ~ TÑt; however, if C varies among years, Ne can be closer to TÑt. Because population regulation affects the genetic contribution of entire cohorts of monocarpic perennials, Ne for these species may be more closely approximated by TÑt than by TN̅ .With density-dependent compensation, and Cov (kt, Nt) \u3c 0 is further reduced because relatively few breeders make a disproportionate contribution to the next generation

Special Issue: Evolutionary perspectives on salmonid conservation and management

This special issue of Evolutionary Applications comprises 15 papers that illustrate how evolutionary principles can inform the conservation and management of salmonid fishes. Several papers address the past evolutionary history of salmonids to gain insights into their likely plastic and genetic responses to future environmental change. The remaining papers consider potential evolutionary responses to climate warming, biological invasions, artificial propagation, habitat alteration, and harvesting. All of these papers consider how such influences might alter selective regimes, which should then favour plastic or genetic responses. Some of the papers then go on to document such responses, at least some of which are genetically based and adaptive. Despite the different approaches and target species, all of the papers argue for the importance of evolutionary considerations in the conservation and management of salmonids

Preserving Nature

To consider the broader environmental significance of protecting species at risk of extinction, we must first consider the roles or functions that species fulfill in nature. Although nature has many definitions, here we define it to mean the end product of ecological and evolutionary processes. That is, within ahabitat, region, or biosphere, the condition of the soil, water, air, and biota reßects the outcome of physical, chemical, ecological, and evolutionary processes. We refer to this combination of abiotic and biotic conditions as nature and to the ecological and evolutionary processes that create it as natural processes. Using these definitions, we propose three approaches in which environmental actions can protect or conserve nature. The first approach is to preserve natural processes by directly managing them or providing suitable substitutions. For example, we can directly manage apolluted watershed to restore its water quality, or we can build expensive water treatment facilities to treat the water (Chichilnisky and Heal1998). The second approach is to protect nature itself, assuming that with adequate protection nature and its natural processes will persist. For example, we can designate marine protected areas that exclude human activities. The third approach is to protect the biotic components of nature that govern the environment. This approach encompasses the intent of the Endangered Species Act (ESA): to protect nature by protecting species. In this chapter, we examine the broader environmental significance of the Endangered Species Act by reviewing the roles species play in natural processes and by examining how natural processes govern our environment, how human activities modify nature, and how the Endangered Species Act can ameliorate the impacts of human activities

Preserving Nature

To consider the broader environmental significance of protecting species at risk of extinction, we must first consider the roles or functions that species fulfill in nature. Although nature has many definitions, here we define it to mean the end product of ecological and evolutionary processes. That is, within ahabitat, region, or biosphere, the condition of the soil, water, air, and biota reßects the outcome of physical, chemical, ecological, and evolutionary processes. We refer to this combination of abiotic and biotic conditions as nature and to the ecological and evolutionary processes that create it as natural processes. Using these definitions, we propose three approaches in which environmental actions can protect or conserve nature. The first approach is to preserve natural processes by directly managing them or providing suitable substitutions. For example, we can directly manage apolluted watershed to restore its water quality, or we can build expensive water treatment facilities to treat the water (Chichilnisky and Heal1998). The second approach is to protect nature itself, assuming that with adequate protection nature and its natural processes will persist. For example, we can designate marine protected areas that exclude human activities. The third approach is to protect the biotic components of nature that govern the environment. This approach encompasses the intent of the Endangered Species Act (ESA): to protect nature by protecting species. In this chapter, we examine the broader environmental significance of the Endangered Species Act by reviewing the roles species play in natural processes and by examining how natural processes govern our environment, how human activities modify nature, and how the Endangered Species Act can ameliorate the impacts of human activities

Harvest-induced evolution and effective population size

Much has been written about fishery-induced evolution (FIE) in exploited species, but relatively little attention has been paid to the consequences for one of the most important parameters in evolutionary biology-effective population size (N-e). We use a combination of simulations of Atlantic cod populations experiencing harvest, artificial manipulation of cod life tables, and analytical methods to explore how adding harvest to natural mortality affects N-e, census size (N), and the ratio N-e/N. We show that harvest-mediated reductions in N-e are due entirely to reductions in recruitment, because increasing adult mortality actually increases the N-e/N ratio. This means that proportional reductions in abundance caused by harvest represent an upper limit to the proportional reductions in N-e, and that in some cases N-e can even increase with increased harvest. This result is a quite general consequence of increased adult mortality and does not depend on harvest selectivity or FIE, although both of these influence the results in a quantitative way. In scenarios that allowed evolution, N-e recovered quickly after harvest ended and remained higher than in the preharvest population for well over a century, which indicates that evolution can help provide a long-term buffer against loss of genetic variability.Peer reviewe

Evolutionary responses by native species to major anthropogenic changes to their ecosystems: Pacific salmon in the Columbia River hydropower system

The human footprint is now large in all the Earth’s ecosystems, and construction of large dams in major river basins is among the anthropogenic changes that have had the most profound ecological consequences, particularly for migratory fishes. In the Columbia River basin of the western USA, considerable effort has been directed toward evaluating demographic effects of dams, yet little attention has been paid to evolutionary responses of migratory salmon to altered selective regimes. Here we make a first attempt to address this information gap. Transformation of the free-flowing Columbia River into a series of slackwater reservoirs has relaxed selection for adults capable of migrating long distances upstream against strong flows; conditions now favour fish capable of migrating through lakes and finding and navigating fish ladders. Juveniles must now be capable of surviving passage through multiple dams or collection and transportation around the dams. River flow patterns deliver some groups of juvenile salmon to the estuary later than is optimal for ocean survival, but countervailing selective pressures might constrain an evolutionary response toward earlier migration timing. Dams have increased the cost of migration, which reduces energy available for sexual selection and favours a nonmigratory life history. Reservoirs are a benign environment for many non-native species that are competitors with or predators on salmon, and evolutionary responses are likely (but undocumented). More research is needed to tease apart the relative importance of evolutionary vs. plastic responses of salmon to these environmental changes; this research is logistically challenging for species with life histories like Pacific salmon, but results should substantially improve our understanding of key processes. If the Columbia River is ever returned to a quasinatural, free-flowing state, remaining populations might face a Darwinian debt (and temporarily reduced fitness) as they struggle to re-evolve historical adaptations

Life-History Divergence In Chinook Salmon: Historic Contingency And Parallel Evolution

By jointly considering patterns of genetic and life-history diversity in over 100 populations of Chinook salmon from California to British Columbia, we demonstrate the importance of two different mechanisms for life history evolution. Mapping adult run timing (the life-history trait most commonly used to characterize salmon populations) onto a tree based on the genetic data shows that the same run-time phenotypes exist in many different genetic lineages. In a hierarchical gene diversity analysis, differences among major geographic and ecological provinces explained the majority (62%) of the overall GST, whereas run-time differences explained only 10%. Collectively, these results indicate that run-timing diversity has developed independently by a process of parallel evolution in many different coastal areas. However, genetic differences between coastal populations with different run timing from the same basin are very modest (GST \u3c 0.02), indicating that evolutionary divergence of this trait linked to reproductive isolation has not led to parallel speciation, probably because of ongoing gene flow. A strikingly different pattern is seen in the interior Columbia River Basin, where run timing and other correlated life-history traits map cleanly onto two divergent genetic lineages (GST ~ 0.15), indicating that some patterns of life-history diversity have a much older origin. Indeed, genetic data indicate that in the interior Columbia Basin, the two divergent lineages behave essentially as separate biological species, showing little evidence of genetic contact in spite of the fact that they co-migrate through large areas of the river and ocean and in some locations spawn in nearly adjacent areas