Abstract: There are currently no policy guidelines for treating hybrids under the U.S. Endangered Species Act (ESA). We considered the scientific basis for determining whether hybridized populations should be included as part of the westslope cutthroat trout (Oncorhynchus clarki lewisi) unit considered for listing under the ESA. Westslope cutthroat trout are threatened by genomic extinction because of widespread introgressive hybridization with introduced rainbow trout (O. mykiss) and Yellowstone cutthroat trout (O. c. bouvieri). Experimental results suggest that first-generation hybrids between westslope cutthroat trout and rainbow trout have reduced fitness. However, hybridization may spread even when hybrids have severely reduced fitness because the production of hybrids is unidirectional÷that is, all the progeny of a hybrid will be hybrids. In addition, heterosis resulting from the sheltering of deleterious recessive alleles in early-generation hybrids may increase the effective rate of introgression. However, such short-term increases in fitness may disrupt important long-term adaptations of native populations. The loss of these adaptations will be difficult to detect because some local adaptations might only be apparent during periodic episodes of extreme environmental conditions, such as winter storms, drought, or fire. Thus, rapid spread of hybridization could result in the loss of local adaptations
in native populations of westslope cutthroat trout and decrease their probability of long-term persistence. Protection of populations with some admixture would protect sources of spreading hybridization. Treatment of hybrids in conservation planning depends primarily on the amount of evolutionary divergence between the hybridizing taxa and the geographical extent of introgression. We recommend that only nonhybridized populations be included as westslope cutthroat trout in the unit to be considered for listing. Populations of unknown status should be protected until more information about these populations becomes available.
Quotes from Text: In this paper, we use the term hybrid to refer to any individual that is either a first generation hybrid or whose recent ancestry (within the last 100 years or so) includes at least one first-generation hybrid individual.
The geographical range for westslope cutthroat trout (WCT) is the largest of all cutthroat trout subspecies and includes the Columbia, Fraser, Missouri, and Hudson Bay drainages of the United States and Canada.
The amount of divergence between WCT and Yellowstone cutthroat trout (YCT) is beyond that usually seen within a single species. For example, it is greater than the divergence at allozyme loci between some species of Pacific salmon.
The WCT exists in sympatry with both resident and anadromous steelhead forms of Columbia River rainbow trout (RT) (O.m.gairdneri) in many drainages throughout the western portion of their range. Nevertheless, the presence of the same fixed genetic differences between WCT and RT in regions of sympatry, as in the rest of the distribution of the WCT, indicates that any natural introgression in these regions of sympatry has been extremely rare. Our genetic analyses of WCT over the last 30 years indicate that natural hybridization between WCT and RT is restricted to the occasional first generation (F1) hybrid individual and rare backcross individuals.
The WCT are threatened by widespread genomic extinction. Epifanio and Phillipp (2001) have defined genomic extinction as loss of lineage (such as WCT) by introgression with another taxon (RT or YCT in this case) or by displacement by a taxon introduced by humans.
Others have used the term genetic extinction for this process. However, genomic is more appropriate than genetic: it is not genes or single locus genotypes that are lost by hybridization. Rather, it is combinations of genotypes over the entire genome that are irretrievably lost. Genomic extinction results in the loss of the legacy of an evolutionary lineage; that is, the genome-wide combination of alleles and genotypes that have evolved over evolutionary time will be lost by introgression with another lineage.
·hybridization has occurred in practically all drainages where rainbow trout were introduced.
Estimates of the current distribution of WCT are highly variable. Liknes and Graham (1988) estimated that nonhybridized WCT populations remained only within 2.5% of their native range in Montana (USA). The status review (USFWS) of the WCT concluded that WCT populations exist in 20% of the stream miles of their historic range.
Native populations of WCT have extreme genetic divergence, even between adjacent tributaries, suggesting that movement and gene flow has been extremely low.
The admixture from RT appears to be increasing the rate of dispersal and thereby causing the spread of introgression. The spread of RT introgression observed·is much greater than that expected from the straying rate of WCT populations.
Recent theoretical work suggests that hybrids may have a short-term fitness advantage because of the sheltering of deleterious recessive alleles with small effects. Natural selection will not be effective in removing slightly deleterious alleles from small populations because of the influence of genetic drift.
Moreover, increases in short-term fitness may disrupt important long-term adaptations. Loss of these adaptations is difficult to detect because some local adaptations of native populations might only be essential during periodic episodes of extreme environmental conditions, such as winter storms, drought, or fire. Weins (1977) argues that short-term studies of fitness and other population characteristics are of limited value because of the importance of ecological crunches in variable environments. For example, Rieman and Clayton (1997) suggest that complex life histories (e.g., mixed migratory behaviors) of bull trout (Salvelinus confluentus) are adaptations to periodic disturbances such as fire that may affect populations only every 25-100 years.
Spread of introgression throughout the range of WCT populations is a major threat to the continued existence of native WCT, regardless of the underlying explanation. The ongoing rapid spread of introgression from RT could result in the loss of local adaptations in native populations of WCT and decrease their probability of long-term persistence.
We present three alternative criteria for including populations in the WCT unit to be considered for listing. Alternatives 1 and 3 are two extreme options for including or not including populations with admixture. Alternative 2 is an intermediate alternative that has been used in several recent management plans.
Alternative 1: Include only Nonhybridized WCT
In the first alternative, only populations that do not show evidence of hybridization from other taxa are included in the WCT unit considered for listing. It is often hard to distinguish between a small proportion of admixture (e.g., <1%) and natural polymorphism that might exist in some populations. Therefore, finding rare alleles at a single marker that suggest hybridization should not be taken as evidence that a population is hybridized. This alternative includes all populations that do not show evidence of hybridization at multiple diagnostic markers. This alternative recognizes that the WCT represents a monophyletic evolutionary lineage isolated from other evolutionary lineages for perhaps 1-2 million years. This is the only alternative that protects the historical evolutionary legacy of WCT. This alternative also protects the local adaptations important for long-term persistence that may be lost through hybridization. Hybrid populations that pose a threat to WCT populations are not eligible for listing and therefore could be managed to reduce ongoing and spreading hybridization.
The disadvantages of including only nonhybridized populations of WCT are associated mainly with small, isolated populations. Many nonhybridized populations of WCT remain, but many of them are isolated headwater populations protected from introgression by a barrier preventing upstream movement (e.g., waterfalls or degraded habitat) and do not have introduced RT or YCT. Extinction threats to these populations are primarily loss of connectivity and potential inbreeding depression. Increasing and improving available habitat increases population sizes and thus decreases threats associated with small, isolated populations. Opportunities to accomplish this at large scales are minimal, however, because of the widespread presence of hybrid swarms throughout the range of WCT.
Alternative 2: Include WCT Populations with Less Than 10% Admixture
The second alternative allows the inclusion of populations that contain up to 10% admixture from RT or YCT in the WCT unit for listing. The value of 10% is arbitrary, but it has been used in recent considerations for the problem. The USFWS status review of WCT used 10% in its estimation of the current distribution of WCT. In addition, a cutthroat management paper developed by an interstate committee of management agencies considered two management components: nonhybridized populations and populations that have the phenotypic attributes of WCT and unique genetic, ecological, or behavioral traits, although they are slightly introgressed (up to 10% admixture). A conservation agreement for WCT in Montana also recommends protecting only populations with limited introgression (up to 10%) because they indicate suitable habitat for WCT or because they may indicate the presence of nonhybridized WCT nearby.
This alternative greatly increases the number of populations considered part of the WCT unit for possible listing. It allows greater connectivity and reduces problems associated with small, isolated populations and inbreeding depression.
Under this alternative, however, populations that do not belong to the evolutionary lineage of WCT are part of the unit to be considered for listing. If WCT are listed, this alternative would protect hybridized populations that serve as a potential source of continued introgression into nonhybridized populations. Allowing genes from YCT or RT to be incorporated into WCT could disrupt coadapted gene complexes that are the product of thousands of generations of selection (outbreeding depression) and could result in the loss of local adaptations in many cases.
Alternative 3: Include all Populations that Retain the Morphological Attributes of WCT
The third alternative allows inclusion in the unit to be considered for listing of all populations that appear to retain phenotypic attributes characteristic of WCT, regardless of their genetic composition. Connectivity among populations is greatest with this alternative. The number of populations included in the unit to be considered for listing increases dramatically.
This alternative has all of the disadvantages of alternative 2. The WCT evolutionary lineage is poorly preserved because many introgressed populations may be protected.
Recommendations
Rates of hybridization and introgression are increasing dramatically worldwide because of translocations of organisms and habitat modification by humans. Hybridization has contributed to extinction of many species through direct and indirect means. Policies should be designed to reduce anthropogenic hybridization.
We believe that only nonhybridized populations should be included as WCT in the unit to be considered for listing under the ESA. Only nonhybridized populations that still contain the WCT genome that has evolved in isolation are likely to possess the local adaptations important for long-term persistence.