Effects of fishing on genetic diversity

9.5.2 Effects of fishing on genetic diversity

Genetic diversity is a rich and irreplaceable part of our heritage. The loss of genetic diversity is highly undesirable, whether the loss is in the form of species extinction or of intraspecific variability. Can fishing itself lead to the loss of genetic varia- tion? The answer must be yes, since fishing re- duces population size from pre-fishing levels and some variation will therefore be lost by genetic drift (see also Reynolds et al., Chapter 15, Volume 2).

In fact, heterozygosity is lost relatively slowly. The expected proportion of the original heterozy- gosity remaining after a bottleneck of size N for

one generation is 1 - 1 – 2 N . A single male and female will thus retain 75% of original heterozygosity, al-

though the loss of heterozygosity compounds with successive generations of size N. A short-term bottleneck will have much less drastic effects than

a long-term bottleneck. Allele loss, however, will

be more striking. Regardless of how many alleles existed at a locus in an ancestral population, a single male and female cannot retain more than four alleles. Rare alleles are likely to be rapidly lost in a bottleneck.

Loss of diversity is commonly observed in hatchery fish and shellfish; it is an expected consequence of genetic drift in small numbers of broodstock. Significant losses arising from fishing pressures will be more noticeable in populations that are already relatively small before fishing; freshwater fish could be particularly vulnerable.

Some weak salmonid subpopulations in a mixed ocean fishery could drop to small N e values, where N e is the biologically effective population size. For- tunately, most wild fisheries are of marine species where populations are generally very large and where there is appreciable gene flow among popu- lations. In such a situation, fishing is unlikely to cause such a massive decrease in population size that an experimentally detectable amount of vari- ability will be lost by drift, at least given sample sizes of the order of 100. A fishery that did reach low population levels would likely become uneco- nomic to exploit, although bycatch harvesting could continue as other species become targeted. The major goal of fisheries management is to maintain populations at levels permitting sustain- able exploitation. However, it would be erroneous to consider marine species as ‘immune’ to genetic depletion (see Ryman et al. 1995 for a full discus- sion), especially if the genetically effective popula- tion size of some species is much less than the apparent size (Hedgecock 1994).

There was some early evidence of a decrease in allozyme heterozygosity concomitant with fishing pressure in the large deepwater orange roughy (Hoplostethus atlanticus) fisheries off New Zealand. This was not attributed to a popula- tion bottleneck but to fishing removing larger and putatively more heterozygous fish (Smith et al. 1991). However, there is no clear relationship be- tween size and heterozygosity in orange roughy (Ward and Elliott 1993), and studies over a longer time period found no correlation between fishing pressure and genetic heterozygosity (Smith and Benson 1997). There was no detectable change in the allozyme heterozygosity of Hawaiian popula- tions of the spiny lobster (Panulirus marginatus) either before or after expansion of the fishery (L.W. Seeb et al. 1990).

Loss of mtDNA diversity has been observed for the New Zealand endemic species Hector’s dolphin (Cephalorhynchus hectori) (Pichler and Baker 2000). A PCR-sequencing protocol was used to compare the mtDNA of museum and contem- porary specimens. The North Island population over the last 20 years has declined from three mtDNA lineages (diversity, h = 0.41) to one (h = 0),

Genetics

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Chapter 9

and the east coast South Island population from

a single captive population appears free of foreign nine lineages (h = 0.65) to five (h = 0.35). Note that genes (Echelle and Echelle 1997). Introduced

values of h can in principle range from 0, where all species may outcompete native species to the individuals are identical, to 1, where all indivi- point that inbreeding becomes a problem in the duals are different. It was suggested that this loss native species – an indirect genetic effect. of diversity resulted from a population decline

Stock enhancement programmes do not intro- caused by dolphin entanglement in gill-nets, a loss duce exotic species but can nevertheless have exacerbated by very low gene-flow rates among unintended deleterious effects. Such programmes populations. The mtDNA F ST of four populations may reintroduce strains from the target area or was high at 0.47, implying little population mix- introduce strains from another part of the species’ ing). Mitochondrial DNA diversity is especially range. These strains are very likely to hybridize sensitive to drift, as a single male and female mat- and introgress with native fish. Again, the fate of ing will transmit only one mtDNA haplotype, and introduced fish can be monitored if they carry the small fragmented populations of this species unique strain-specific markers. Allozyme studies make it particularly vulnerable to genetic loss.

have confirmed introgression, for example in European brown trout (Salmo trutta) restocking

9.5.3 programmes. In Spain, local stock heterogeneity is Genetic effects of stocking

being eroded by introductions of hatchery-reared There are two major classes of stocking pro- fish (Machordom et al. 1999), and in Switzerland grammes for fish:

introduced trout of Atlantic basin origin are re-

1 those where exotic species are introduced to placing native Adriatic strains S. trutta fario and S. areas where they have never naturally existed;

trutta marmoratus (Largiader and Scholl 1995).

2 those designed to enhance pre-existing fisheries. Clearly, where possible, enhancement should be The latter may be enacted to replace a locally of local rather than exotic strains. Even then, the extinct stock, to rebuild a collapsed stock or to introduced strains are likely to be of hatchery augment a natural population for recreational fish- origin and therefore will have undergone some ing. While stocking programmes may have major change in genetic make-up with respect to ances- benefits, they may also have very significant detri- tral populations. mental outcomes (see Cowx, Chapter 17, Volume

One undesirable consequence of such 2). Introduction of exotic species can lead to the hybridization is that locally coadapted gene com- elimination of native species, hybridization with plexes, which will be a particular genetic make- native species, habitat alteration and the spread up favoured by selection in that location, can of disease. Stock enhancement programmes can break down, reducing fitness. Such outbreeding introduce disease and can deleteriously affect the depression has been recorded for pink salmon gene pool of native fish. Cowx (1998) provides a (Oncorhynchus gorbuscha) (Gharrett and Smoker recent collection of papers on fish stocking.

1991). Hatchery-bred rainbow trout, marked by a

Introductions of exotic species to habitats rare allozyme variant, had a reproductive success occupied by a closely related species can lead to only 28% that of wild trout, but so outnumbered hybridization and introgression, problems readily native fish that 62% of smolts were offspring of monitored by species-diagnostic loci. In Arizona, naturally spawning hatchery trout (Chilcote et al. the gene pool of the Apache trout (Oncorhynchus 1986). There is ‘compelling evidence’ that apache ) has been threatened by hybridizations hatchery production of at least three species of with introduced non-native cutthroat (O. clarki) Pacific salmonids lowers fitness, and that when and rainbow (O. mykiss) trout (Carmichael et al. such fish hybridize with wild fish, the productivity 1993). All wild populations of the leon springs pup- and viability of the naturally spawning popula- fish (Cyprinodon bovinus) have been introgressed tions declines substantially (Reisenbichler and by introduced sheepshead minnow (C. variegatus); Rubin 1999).

There may also be indirect genetic effects of enhancement programmes. One example con- cerns introductions of Atlantic salmon (Salmo salar ) genetically resistant to but carrying an ec- toparasite; the recipient population was suscepti- ble, causing heavy mortality of native fish (Bakke 1991).

A particular threat to the genetic integrity and viability of wild fish populations may come from the deliberate or accidental release of genetically engineered or transgenic fish (Reichhardt 2000). Such fish are likely to be engineered for higher growth rate by elevating growth hormone (GH) levels. The effects of such fish on native popula- tions remain unknown. They are often assumed to have reduced viability, but GH-enhanced transgenic coho salmon (Oncorhynchus kisutch) showed a marked competitive feeding advantage over non-transgenic fish (Devlin et al. 1999). Thus, depending of course on other fitness-related traits, escaped GH transgenic fish may be able to compete successfully in the wild with native non- transgenic fish. Even if the transgene does lower viability, modelling studies (Muir and Howard 1999) have shown that it can still spread if it simul- taneously increases male mating success, for ex- ample by yielding faster-growing larger males. This can, in principle, lead to local extinction. It seems that in order to minimize the genetic effects of escapees on local populations, commercial pro- ducers of transgenic fish will have to guarantee that the transgenic product is sterile. This might

be achievable through the production of triploid fish or by inclusion of a transgene for repressible sterility (Grewe et al. submitted). Containment fa- cilities would still be advisable; the release of large numbers of voraciously feeding, rapidly growing, GH-enhanced fish could seriously disrupt the functioning of natural ecosystems, even if the fish were sterile.