Loss of Genetic Diversity Among Managed Populations

Loss of Genetic Diversity Among Managed Populations
		by *David P. Philipp* Illinois Natural History Survey *Julie E. Claussen* Illinois Natural History Survey
Species are composed of genetically divergent units usually interconnected by some (albeit low) level of gene flow (Soulé 1987). Because of this restriction in gene flow, natural selection can genetically tailor populations to their environments through the process of local adaptation (Wright 1931).
Because freshwater and anadromous (i.e., adults travel upriver from the sea to spawn) fishes are restricted by the boundaries of their aquatic habitats, genetic subdivisions may be more pronounced for these vertebrates than for others. Consequently, managers of programs for these species must realize that the stock (i.e., local discrete populations), and not the species as a whole, must be the units of primary management concern (Kutkuhn 1981).
Genetic variability in a species occurs both among individuals within populations as well as among populations (Wright 1978). Variation within populations is lost through genetic drift (see glossary; Allendorf et al. 1987), a process increased when population size becomes small. Variation among populations is lost when previously restricted gene flow between populations is increased for some reason (e.g., stocking, removal of natural barriers such as waterfalls); differentiation between populations is lost as a result of the homogenization of two previously distinct entities (Altukhov and Salmenkova 1987; Campton 1987).
Beyond this loss of genetic variation, mixing two groups can result in outbreeding depression, which is the loss of fitness in offspring that results from the mating of two individuals that are too distantly related (Templeton 1987). This loss in fitness is caused by the disruption of the process that produced advantageous local adaptations through natural selection. Inbreeding depression, on the other hand, is the loss of fitness produced by the repeated crossing of related organisms. The area of optimal relatedness occurs between inbreeding depression and outbreeding depression.
Loss of Genetic Integrity Through Stocking
Many sportfish populations are managed by using a combination of harvest regulation, habitat manipulation, and stocking. Jurisdiction for these activities falls to federal, state, tribal, and local governments, as well as private citizens. Many resource managers in the past were unaware of the long-term consequences that stocking efforts would have on the genetic integrity of local populations (Philipp et al. 1993).
Fish introductions can be classified into three types: non-native introductions, in which a given species of fish is introduced into a body of water outside its native range (regardless of any political boundaries); stock transfers, in which fish from one stock are introduced into a water body in a different geographic region inhabited by a different stock of that same species, yet are still within their native range; and genetically compatible introductions, in which fish are removed from a given water body and they, or more often their offspring, are introduced back into that water body or another water body that is still within the boundaries of the genetic stock serving as the hatchery brood source (Philipp et al. 1993).
Although non-native introductions may often cause ecological problems for the environments in which they are introduced, they can also cause genetic problems if they hybridize with closely related native species. Examples of this are the hybridization of introduced smallmouth bass (Micropterus dolomieu) and spotted bass (M. punctulatus) with native Guadalupe bass (M. treculi) in Texas (Morizot et al. 1991), and the hybridization of introduced rainbow trout (Oncorhynchus mykiss) with native Apache trout (O. apache; Carmichael et al. 1993). The greatest degree of genetic damage, that is, the loss of genetic variation among populations, is caused by stock transfers, a common practice among fisheries management agencies and the private sector.
Largemouth Bass

Largemouth bass (Micropterus salmoides) exemplify how introduction programs cause the loss of genetic diversity. The original range of the largemouth bass was restricted to parts of the central and southeastern United States (Figure), extending northward into some of southern Ontario (MacCrimmon and Robbins 1975). Bailey and Hubbs (1949), however, described two subspecies. The Florida subspecies, M.s. floridanus, was formerly restricted to much of peninsular Florida (Figure, a), whereas the range of the northern subspecies, M.s. salmoides, extended north and west of an intergrade zone that included parts of South Carolina, Georgia, Alabama, and northern Florida. It is likely, though, that the intergrade zone had already been expanded from the original natural hybrid zone as a result of early fish stocking programs.

Since 1949, however, much more serious stocking efforts have extended this intergrade zone. A survey of largemouth bass populations conducted in the late 1970's (Philipp et al. 1983) revealed that the intergrade zone had grown considerably larger through the deliberate stocking efforts of the involved state agencies (Figure, b). Additional introductions of M.s. floridanus since that genetic survey have now spread the genes of that subspecies across the entire southern range of M.s. salmoides (Figure, c).

This introduction of the Florida largemouth has compromised the genetic integrity of all the populations of the northern largemouth bass into which the species has been introduced (populations in Texas, Oklahoma, Arkansas, Louisiana, Mississippi, Tennessee, Alabama, Georgia, South Carolina, North Carolina, Virginia, and Maryland, at a minimum). Those now-genetically mixed populations have lost much of their distinctness because of the loss of among-population genetic variation that accompanies this type of homogenization. Populations other than those in the water bodies actually stocked will be affected as well because of inevitable gene flow into and between other connected populations. As a result, genetic integrity is now at risk for all populations of this important sportfish species throughout the southern and eastern portions of its native range.

Figure. Loss of genetic variation among largemouth bass populations. a. The native range of the largemouth bass (Micropterus salmoides) is delineated by the red lines (MacCrimmon and Robbins 1975). As first described by Bailey and Hubbs (1949), the Florida subspecies, M.s. floridanus, was restricted to peninsular Florida (blue); the northern subspecies, M.s. salmoides, covered most of the rest of the range of the species; and there was a relatively small intergrade zone between the two resulting from some indeterminable combination of natural hybridization and human-caused mixing of stocks. b. The expansion of the intergrade by 1980 was described by Philipp et al. (1983). Because detailed ranges were not explored in all states, and because this intergrade zone expansion was likely caused by state stocking programs, entire states are classified according to whether the intergrade zone was expanded. c. The current intergrade zone is now even larger because of the addition of more states in which largemouth bass containing at least some M.s. floridanus genes are being introduced either by the state fish and game agencies themselves or by private groups. Notice that the entire southern and eastern portion of the original range of the northern subspecies, M.s. salmoides, is at risk of being inundated with M.s. floridanus genes.

In addition, because the two subspecies have quite different characteristics (Cichra et al. 1982; Fields et al. 1987; Kleinsasser et al. 1990), these massive stock transfers will likely result in outbreeding depression. More specifically, the Florida subspecies exhibits significantly poorer survival, growth, and reproductive success in Illinois than does the northern subspecies (Philipp 1991; Philipp and Whitt 1991). Also, the offspring resulting from crossing the two subspecies (in either direction) are less fit in Illinois than are the offspring of the pure northern subspecies (Philipp 1991). These results extend to populations of the northern subspecies across its range from Texas to Minnesota (unpublished data).
Conclusions
The genetic integrity of largemouth bass stocks, and likely of many other managed fish species as well, is eroding as a result of management programs that inadvertently permit or deliberately promote stock transfers. This causes not only the loss of genetic variation among populations, but through outbreeding depression it is also probably negatively affecting the fitness of many native stocks involved. We need to address genetic integrity when restoring native populations.
		For further information: David P. Philipp Illinois Natural History Survey Center for Aquatic Ecology 607 E. Peabody Dr. Champaign, IL 61820

References
Allendorf, F.W., N. Ryman, and F.M. Utter. 1987. Genetics and fishery management past, present, and future. Pages 1-19 in N. Ryman and F.M. Utter, eds. Population genetics and fishery management. Washington Sea Grant Program, Seattle. Altukhov, Y.P., and E.A. Salmenkova. 1987. Stock transfer relative to natural organization, management and conservation of fish populations. Pages 333-344 in N. Ryman and F.M. Utter, eds. Population genetics and fishery management. Washington Sea Grant Program, Seattle. Bailey, R.M., and C.L. Hubbs. 1949. The black basses (Micropterus) of Florida, with description of a new species. University of Michigan Museum of Zoology Occasional Papers 516:1-40. Campton, D.E. 1987. Natural hybridization and introgression in fishes: methods of detection and interpretation. Pages 161-192 in N. Ryman and F.M. Utter, eds. Population genetics and fishery management. Washington Sea Grant Program, Seattle. Carmichael, G.J., J.N. Hanson, M.E. Schmidt, and D.C. Morizot. 1993. Introgression among Apache, cutthroat, and rainbow trout in Arizona. Transactions of the American Fisheries Society 122:121-130. Cichra, C.E., W.H. Neill, and R.L. Noble. 1982. Differential resistance of northern and Florida largemouth bass to cold shock. Proceedings of the Southeastern Association of Fish and Wildlife Agencies 34(1980):19-24. Fields, R., S.S. Lowe, C. Kaminski, G.S. Whitt, and D.P. Philipp. 1987. Critical and chronic thermal maxima of northern and Florida largemouth bass and their reciprocal F₁ and F₂ hybrids. Transactions of the American Fisheries Society 116:856-863. Kleinsasser, L.J., J.H. Williamson, and B.G. Whiteside. 1990. Growth and catchability of northern Florida and F₁ hybrid largemouth bass in Texas ponds. North American Journal of Fisheries Management 10:462-468. Kutkuhn, J.H. 1981. Stock definition as a necessary basis for cooperative management of Great Lakes fish resources. Canadian Journal of Fisheries and Aquatic Sciences 38:1476-1478.	MacCrimmon, H.R., and W.H. Robbins. 1975. Distribution of the black basses in North America. Pages 56-66 in R.H. Stroud and H. Clepper, eds. Black bass biology and management. Sport Fishing Institute, Washington, DC. Morizot, D.C., S.W. Calhoun, L.L. Clepper, M.E. Schmidt, J.H. Williamson, and G.J. Carmichael. 1991. Multispecies hybridization among native and introduced centrarchid basses in central Texas. Transactions of the American Fisheries Society 120:283-289. Philipp, D.P. 1991. Genetic implications of introducing Florida largemouth bass, Micropterus salmoides floridanus. Canadian Journal of Fisheries and Aquatic Sciences 48(1):58-65. Philipp, D.P., W.F. Childers, and G.S. Whitt. 1983. A biochemical genetic evaluation of the northern and Florida subspecies of largemouth bass. Transactions of the American Fisheries Society 112:1-20. Philipp, D.P., J.M. Epifanio, and M.J. Jennings. 1993. Conservation genetics and current stocking practices: are they compatible? Fisheries 18:14-16. Philipp, D.P., and G.S. Whitt. 1991. Survival and growth of northern, Florida, and reciprocal F₁ hybrid largemouth bass in central Illinois. Transactions of the American Fisheries Society 120:156-178. Soulé, M.E., ed. 1987. Conservation biology: the science of scarcity and diversity. Sinauer Associates, Inc., Sunderland, MA. 584 pp. Templeton, A.R. 1987. Coadaptation and outbreeding depression. Pages 105-116 in M.E. Soulé, ed. Conservation biology: the science of scarcity and diversity. Sinauer Associates, Inc., Sunderland, MA. Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97-159. Wright, S. 1978. Evolution and the genetics of populations. Vol. 4. Variability within and among natural populations. University of Chicago Press, IL.

References

Allendorf, F.W., N. Ryman, and F.M. Utter. 1987. Genetics and fishery management past, present, and future. Pages 1-19 in N. Ryman and F.M. Utter, eds. Population genetics and fishery management. Washington Sea Grant Program, Seattle.

Altukhov, Y.P., and E.A. Salmenkova. 1987. Stock transfer relative to natural organization, management and conservation of fish populations. Pages 333-344 in N. Ryman and F.M. Utter, eds. Population genetics and fishery management. Washington Sea Grant Program, Seattle.

Bailey, R.M., and C.L. Hubbs. 1949. The black basses (Micropterus) of Florida, with description of a new species. University of Michigan Museum of Zoology Occasional Papers 516:1-40.

Campton, D.E. 1987. Natural hybridization and introgression in fishes: methods of detection and interpretation. Pages 161-192 in N. Ryman and F.M. Utter, eds. Population genetics and fishery management. Washington Sea Grant Program, Seattle.

Carmichael, G.J., J.N. Hanson, M.E. Schmidt, and D.C. Morizot. 1993. Introgression among Apache, cutthroat, and rainbow trout in Arizona. Transactions of the American Fisheries Society 122:121-130.

Cichra, C.E., W.H. Neill, and R.L. Noble. 1982. Differential resistance of northern and Florida largemouth bass to cold shock. Proceedings of the Southeastern Association of Fish and Wildlife Agencies 34(1980):19-24.

Fields, R., S.S. Lowe, C. Kaminski, G.S. Whitt, and D.P. Philipp. 1987. Critical and chronic thermal maxima of northern and Florida largemouth bass and their reciprocal F₁ and F₂ hybrids. Transactions of the American Fisheries Society 116:856-863.

Kleinsasser, L.J., J.H. Williamson, and B.G. Whiteside. 1990. Growth and catchability of northern Florida and F₁ hybrid largemouth bass in Texas ponds. North American Journal of Fisheries Management 10:462-468.

Kutkuhn, J.H. 1981. Stock definition as a necessary basis for cooperative management of Great Lakes fish resources. Canadian Journal of Fisheries and Aquatic Sciences 38:1476-1478.

MacCrimmon, H.R., and W.H. Robbins. 1975. Distribution of the black basses in North America. Pages 56-66 in R.H. Stroud and H. Clepper, eds. Black bass biology and management. Sport Fishing Institute, Washington, DC.

Morizot, D.C., S.W. Calhoun, L.L. Clepper, M.E. Schmidt, J.H. Williamson, and G.J. Carmichael. 1991. Multispecies hybridization among native and introduced centrarchid basses in central Texas. Transactions of the American Fisheries Society 120:283-289.

Philipp, D.P. 1991. Genetic implications of introducing Florida largemouth bass, Micropterus salmoides floridanus. Canadian Journal of Fisheries and Aquatic Sciences 48(1):58-65.

Philipp, D.P., W.F. Childers, and G.S. Whitt. 1983. A biochemical genetic evaluation of the northern and Florida subspecies of largemouth bass. Transactions of the American Fisheries Society 112:1-20.

Philipp, D.P., J.M. Epifanio, and M.J. Jennings. 1993. Conservation genetics and current stocking practices: are they compatible? Fisheries 18:14-16.

Philipp, D.P., and G.S. Whitt. 1991. Survival and growth of northern, Florida, and reciprocal F₁ hybrid largemouth bass in central Illinois. Transactions of the American Fisheries Society 120:156-178.

Soulé, M.E., ed. 1987. Conservation biology: the science of scarcity and diversity. Sinauer Associates, Inc., Sunderland, MA. 584 pp.

Templeton, A.R. 1987. Coadaptation and outbreeding depression. Pages 105-116 in M.E. Soulé, ed. Conservation biology: the science of scarcity and diversity. Sinauer Associates, Inc., Sunderland, MA.

Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:97-159.

Wright, S. 1978. Evolution and the genetics of populations. Vol. 4. Variability within and among natural populations. University of Chicago Press, IL.

Loss of Genetic Diversity Among Managed Populations

Loss of Genetic Integrity Through Stocking

Largemouth Bass

Conclusions