Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild

Araki, Hideki; Cooper, Becky; Blouin, Michael S.

doi:10.1098/rsbl.2009.0315

Cited by 215 publications

(251 citation statements)

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“…We genotyped all samples at eight highly polymorphic microsatellite loci (Omy 1001, Omy 1011, Omy 1191, Omy77, One108, One2, Ssa407 and Str2), which average 36 alleles per locus (see Araki et al, 2007a,b for details of microsatellite loci, Hardy-Weinberg proportions and molecular methods). These data were previously employed to determine the relative reproductive success of hatchery and wild steelhead (Araki et al, 2007a,b), and of wild-born steelhead having hatchery vs wild parents (Araki et al, 2009). Results from this work documented that hatchery fish created with two wild parents averaged 85% the reproductive success of their wild counterparts and that an additional generation in captivity reduced fitness in the wild by an additional 50% (Araki et al, 2007a).…”

Section: Sample Collection and Typingmentioning

confidence: 64%

“…After returning from the ocean, a portion (or in many cases all) of the returning adult hatchery fish are allowed onto the spawning grounds with the wild-born fish. Wild broodstock are preferred in some supplementation programs because they can produce offspring that have much higher fitness in the wild than offspring from older, domesticated hatchery stocks (though even first generation hatchery fish can have reduced fitness in the wild; Araki et al, 2007a;Araki et al, 2009;Williamson et al, 2010;Berntson et al, 2011;Theriault et al, 2011;Christie et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Effective size of a wild salmonid population is greatly reduced by hatchery supplementation

et al. 2012

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Many declining and commercially important populations are supplemented with captive-born individuals that are intentionally released into the wild. These supplementation programs often create large numbers of offspring from relatively few breeding adults, which can have substantial population-level effects. We examined the genetic effects of supplementation on a wild population of steelhead (Oncorhynchus mykiss) from the Hood River, Oregon, by matching 12 run-years of hatchery steelhead back to their broodstock parents. We show that the effective number of breeders producing the hatchery fish (broodstock parents; N b ) was quite small (harmonic mean N b ¼ 25 fish per brood-year vs 373 for wild fish), and was exacerbated by a high variance in broodstock reproductive success among individuals within years. The low N b caused hatchery fish to have decreased allelic richness, increased average relatedness, more loci in linkage disequilibrium and substantial levels of genetic drift in comparison with their wild-born counterparts. We also documented a substantial Ryman-Laikre effect whereby the additional hatchery fish doubled the total number of adult fish on the spawning grounds each year, but cut the effective population size of the total population (wild and hatchery fish combined) by nearly two-thirds. We further demonstrate that the Ryman-Laikre effect is most severe in this population when (1) 410% of fish allowed onto spawning grounds are from hatcheries and (2) the hatchery fish have high reproductive success in the wild. These results emphasize the trade-offs that arise when supplementation programs attempt to balance disparate goals (increasing production while maintaining genetic diversity and fitness).

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Section: Sample Collection and Typingmentioning

confidence: 64%

Section: Introductionmentioning

confidence: 99%

Effective size of a wild salmonid population is greatly reduced by hatchery supplementation

et al. 2012

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“…Finally, re duced genetic diversity among individuals can arise due to founder effects, small effective population sizes and genetic drift (see Bekkevold et al 2006, Hutchings & Fraser 2008 for reviews and Pampoulie et al 2006, Glover et al 2010 for examples in cod). In this context, one of the main ecological concerns is that escapee fish hybridize with wild populations leading to introgression of farmed genetic material into the wild pool (as observed in some Norwegian Atlantic salmon populations by Glover et al 2012Glover et al , 2013, potentially lowering wild stock fitness and/or causing the extinction of the original wild genotypes (reviewed by Fleming 1995, Weir & Grant 2005, Ferguson et al 2007, Hutchings & Fraser 2008; see Araki et al 2009 for a study in a fish population). As an example, in Atlantic salmon, interbreeding and competition be tween farmed and wild individuals causes lower fitness and productivity of wild populations (Fleming et al 2000, McGinnity et al 2003, even though this effect seems to be family specific .…”

Section: Introductionmentioning

confidence: 99%

Wild Atlantic cod sperm motility is negatively affected by ovarian fluid of farmed females

Beirão¹,

Purchase²,

Wringe³

et al. 2014

Aquacult. Environ. Interact.

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Atlantic cod escape from fish farms at higher rates than commonly cultured marine species, and escapees have been observed to interact with wild fish in mating aggregations. Previous research suggests that potential interbreeding is mediated largely by the likelihood of wild males spawning with escaped females, and as such, the egg and ovarian fluid characteristics of these females could affect fertilization success and the likelihood of hybridization. Farmed cod have been noted to have poor egg quality compared to wild individuals, and some of this difference may be due to the ovarian fluid, which can affect key sperm-motility parameters related to fertilization success. We tested the hypothesis that the ovarian fluid of farmed females negatively affects the sperm performance of wild males. Sperm-motility parameters and fertilization capacity of wild male sperm were analyzed in the presence of both farmed and wild female ovarian fluid. Sperm performed similarly in the presence of wild female ovarian fluid and a seawater control. Ovarian fluid of farmed females negatively affected sperm swimming and the capacity to fertilize eggs. These differences may be related to nutritional deficiencies of farmed individuals. Although it has been demonstrated that wild males actively court farmed females, our results indicate that their ovarian fluid quality can inhibit fertilization success.

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“…Ecologists, conservationists, and wildlife managers alike should be aware of the quality/type of habitat that individuals come from and the possibility of unexpected dynamics in focus areas caused by carryover effects of natal habitats on immigrating individuals. This aspect highlights a possible difficulty in identifying carryover effects in nature, given that it could be critical to know where dispersing individuals come from and what conditions they experienced to identify potential carryover effects when natal and new habitats differ (16,30,48,52,53). Furthermore, carryover effects can alter dispersal decisions and capabilities (16,44).…”

Section: Methodsmentioning

confidence: 99%

Carryover effects drive competitive dominance in spatially structured environments

Allen

Rudolf

2016

Proc. Natl. Acad. Sci. U.S.A.

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Understanding how changes to the quality of habitat patches affect the distribution of species across the whole landscape is critical in our human-dominated world and changing climate. Although patterns of species' abundances across a landscape are clearly influenced by dispersal among habitats and local species interactions, little is known about how the identity and origin of dispersers affect these patterns. Because traits of individuals are altered by experiences in their natal habitat, differences in the natal habitat of dispersers can carry over when individuals disperse to new habitats and alter their fitness and interactions with other species. We manipulated the presence or absence of such carried-over natal habitat effects for up to eight generations to examine their influence on two interacting species across multiple dispersal rates and different habitat compositions. We found that experimentally accounting for the natal habitat of dispersers significantly influenced competitive outcomes at all spatial scales and increased total community biomass within a landscape. However, the direction and magnitude of the impact of natal habitat effects was dependent upon landscape type and dispersal rate. Interestingly, effects of natal habitats increased the difference between species performance across the landscape, suggesting that natal habitat effects could alter competitive interactions to promote spatial coexistence. Given that heterogeneity in habitat quality is ubiquitous in nature, natal habitat effects are likely important drivers of spatial community structure and could promote variation in species performance, which may help facilitate spatial coexistence. The results have important implications for conservation and invasive species management.carryover effects | natal habitat effect | competition | metacommunity | dispersal C ommunities do not exist in a vacuum; instead, they are connected to each other through dispersal of interacting species. Consequently, dispersal among different kinds of habitat patches is increasingly recognized as a key factor driving the dynamics and structure of communities from local to regional spatial scales (1-5). In classic models, the persistence and dynamics of populations within a patch are determined by two factors: the rate of dispersal between patches of habitat and the species fitness within each local patch (6-8). This view has persisted into metacommunity theory (multiple communities connected by dispersal of individuals between the patches of habitat they occur in) as well, where the influence of dispersers on community dynamics is generally considered only in terms of their numbers (i.e., dispersal rate) and habitat-specific performance (1, 9-11). Implicit in this case, and for most of spatial ecology, is that the interactions and population dynamics within a habitat are solely determined by the quality of that habitat. However, this approach ignores the often substantial variation in individual traits and fitness within and across habitats in a natural sys...

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Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild

Cited by 215 publications

References 12 publications

Effective size of a wild salmonid population is greatly reduced by hatchery supplementation

Effective size of a wild salmonid population is greatly reduced by hatchery supplementation

Wild Atlantic cod sperm motility is negatively affected by ovarian fluid of farmed females

Carryover effects drive competitive dominance in spatially structured environments

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