The management of small, isolated salmonid populations: do we have to fix it if it ain't broken?

Abstract

In their recent paper, Sato H Gharrett et al., 1999; McGinnity et al., 2003; Tallmon et al., 2004), but claimed the close geographical proximity, similar habitat and small genetic differences among remnant populations might considerably reduce this risk. In a recent review, Edmands (2007) stated that concerns over outbreeding should be taken seriously, as the effects of outbreeding can be, in some cases, as damaging as severe inbreeding. Here, we raise concerns about mixing of populations as a strategy to increase genetic variation, and we bring evidence of likely outbreeding depression observed in the rehabilitation project of the endangered freshwater salmonid marble trout Salmo marmoratus, started in Slovenia in 1993 (Crivelli et al., 2000). Since the beginning of the rehabilitation project, four marble trout populations went extinct due to landlsides (Predelica) and severe flood events (Gorska, Sventarska and Zakojska). The seven remnant populations of marble trout living in Slovenian streams are genetically distant (FST=0.66, Fumagalli et al., 2002), present a very low effective population size (for the Huda Grapa population a total population size ranging from 29 to 60 individuals was estimated between 2000 and 2007) and very low genetic variability estimated at 14 microsatellite loci (for Huda Grapa Ho=0.046, Fumagalli et al., 2002). In order to expand the genetic variability of marble trout living in the watershed, a new population (Gatsnik) was created in 1998 in a previously fishless stream by mixing the progeny of marble trout from two remnant populations from isolated streams with similar habitat (Trebuscica and Lipovesck). After two generations, the population of Gatsnik presented the typical features associated with maladaptation and outbreeding depression, that is lower annual survival rate (0.39 0.02 for trout born in the stream, higher than 0.55 for other marble trout populations living in the study area, Vincenzi et al., 2008), reproductive underperformance at the F2 generation and unusual morphological abnormalities (Fig. 1). Moreover, preliminary results from a egg-to-fry experiment performed in the fish farm for the F1 generation of Gatsnik showed 80.4% of mortality from fertilization to hatching (35.6 29.2% for the remnant populations) (D. Jesensek, pers. comm.). The translocation experiment in Gatsnik is still ongoing and may provide unequivocal evidence of outbreeding effects in 3–4 years. Nevertheless, despite the striking contrast of salmonid species in lifehistory traits may hinder generalizations, what we observed in the marble trout population of Gatsnik urges now further considerations on the opportunity of mixing populations of salmonids to increase their genetic variability. As recently reviewed by Willi et al. (2006), small populations are predicted to have low potential to adapt to environmental changes, as genetic variation and potential response to selection should be positively related to population size. Moreover, individuals in small populations may have lower fitness and be inbred, which may decrease an adaptive response to unpredictable environmental changes. Apart from the obvious cases of overexploitation, pollution and human-induced fragmentation, the small population size and low heterozygosity frequently observed in endemic