A systematic review of phenotypic responses to between-population outbreeding (systematic review)
The translocation of plants or animals between populations has been used in conservation to reinforce populations of threatened species, and may be used in the future to buffer species’ ranges from the anticipated effects of environmental change. This population admixture can result in outbreeding, and the resulting “hybrid” offspring can be either fitter (heterosis) or less fit (outbreeding depression) than their parents. Outbreeding depression has the potential to undermine conservation plans that mix populations of declining or threatened species.
We searched for literature documenting phenotypic responses to intraspecific outbreeding between natural populations of animal and plant species. Outbreeding responses were summarised as log-response ratios that compared hybrid with mid-parent phenotypes (528 effect sizes from 98 studies). These data included effect sizes from both fitness components (survival, viability and fecundity traits) and other traits (e.g. morphological, physiological, defence), and were pooled using Bayesian mixed-effects meta-analysis.
There was no overall effect of outbreeding on hybrid phenotypes (overall pooled effect = +2.61% phenotypic change relative to parents, 95% credible interval (CI) −1.03–6.60%). However, fitness component traits responded significantly more negatively to outbreeding than traits less directly linked with fitness. Our model predicted a significant 6.9% F1 generation benefit to outcrossing through non-fitness traits (CI 2.7–11.2%), but no significant benefit to these traits in the F2 (3.5%; CI −4.3–12.2%). Fitness component traits were predicted to suffer a cost (−8.8%) relative to parents in the F2 (CI −14.1– − 2.5%), but not in the F1 (+1.3%; CI −2.1–5.4%). Between-study variation accounted for 39.5% of heterogeneity in outbreeding responses, leaving 27.1% of heterogeneity between effect sizes within studies and 33.4% attributable to measurement error within effect sizes.
Our study demonstrates consistent effects of trait type on responses to intraspecific outbreeding, and indicates the potential for outbreeding depression in the F2. However, our analyses also reveal significant heterogeneity in outbreeding responses within and among studies. Thus, outbreeding costs will not always occur. Conservation practitioners may be able to anticipate when such outbreeding depression should arise using an existing decision-making framework that takes into account the context of hybridising populations.
Outbreeding Depression, Heterosis, Phenotypic Response, Conservation Genetics, Line-cross Analysis, Outbreeding, Outcrossing, Intraspecific Hybridisation
Genetic diversity is important for the sustainability of populations of living organisms. It provides the raw genetic material upon which natural selection can act in order to adapt them to changes in their environment (including current anthropogenic changes such as increased nitrogen deposition and climate change). For many taxa, genetic diversity is also important for the avoidance of inbreeding depression, which is the decline in fitness of offspring associated with sexual reproduction among related individuals. Inbreeding depression becomes more likely as populations become smaller in size and may contribute to the extinction of small populations (Reed and Frankham, 2003, O’Grady et al., 2006).
The need to equip natural populations with sufficient genetic variation for conservation purposes has been recognized for some time (Frankel, 1974, Frankel and Soulé, 1981), and a compelling body of evidence exists in the scientific literature documenting the detrimental effects of inbreeding depression in wild populations (reviewed in Crnokrak and Roff, 1999). A classic example is the case of the Florida panther, whose population had declined to a perilously small size by the latter part of the 20th century (Roelke et al., 1993). Individuals of this population suffered problems such as poor sperm quality, kinked tails and un-descended testicles, maladies that were attributed to the effects of inbreeding depression (Roelke et al., 1993) and reduced the chances of population survival and recovery. During 1995 individuals were translocated to the Florida population from a distinct population in Texas. Offspring descended from the mixed population had a much reduced occurrence of the detrimental phenotypes exhibited in the population prior to the translocation event (Land et al., 2001) and contributed to a subsequent recovery in numbers (Pimm et al., 2006). This effect of fitness recovery after translocation is termed “genetic rescue”, and has been observed in diverse taxa, for example, in fish (Vrijenhoek, 1994), birds (Westemeier et al., 1998) and plants (Willi et al., 2007) .
Despite the potential benefits (especially to small populations of naturally out-breeding species) of creating hybrid populations, the conservation movement remains cautious about applying population translocations widely as a tool to enhance population sustainability (Gregory et al., 2006). This caution is well founded, since it has been shown that in some circumstances, population hybridisation can lead to a reduction in fitness of the mixed population after translocation, called outbreeding depression. The basis of such a fitness reduction is that populations being mixed may have become adapted to the specific environments in which they exist, and/ or they may have diverged genetically such that genomic incompatibilities are exposed upon population mixing. A well-known example of this phenomenon is the reduction in fitness that can be observed in offspring derived from mating between individuals of different species (Arnold and Hodges, 1995). Within species it is expected that the extent and duration of outbreeding depression will depend on factors such as the physical, genetic and ecological distance amongst populations that become admixed (Edmands, 2002). For example, it is widely assumed that geographical distance between populations is a surrogate for the environmental (climatic, ecological) similarity among sites occupied by populations, and thus serves as a proxy for the potential adaptive differential between them. A further factor influencing the extent of local adaptation within and among populations is the degree of population connectivity, or gene-flow between them, related to the dispersal capacity and mating system of the species under consideration. Where migration among populations is high, the genetic composition of populations will become more homogeneous, potentially hindering the development of local adaptation (Storfer, 1999). The severity of outbreeding depression may also decline as natural selection begins to act upon the expanded pool of genetic variation that has been created by a hybridisation event (e.g. Carney et al., 2000), removing maladapted individuals and adapting the mixed population to its environment.
There are a number of reasons why conservation managers may choose to translocate or not to translocate individuals in order to reinforce a population that is in decline. These include, in addition to the scientific arguments outlined above, economic considerations and concerns that translocations may destroy the unique features of threatened populations that constitute biological heritage. There is also a risk that translocation might encourage the spread of parasites or disease. Finally, the conservation manager must take into account the possibility that in avoiding translocation, the threatened population may lack the genetic variability necessary for adaptation to future environmental changes. The scientific arguments for and against population reinforcement by translocation are currently of great interest to conservation practitioners (Gregory et al., 2006) and are also hotly debated, with different NGOs taking very different viewpoints about this problem. A growing body of evidence exists on outbreeding-depression, and it is in the interest of the conservation community that this evidence should be synthesized and disseminated so that conservation actions may be enhanced and guided by the best available evidence.
The aim of this review is to ask whether we can defend scientifically the position of avoiding population mixture by translocation because of possible differences in local adaptation between the source populations. Does outbreeding depression (as a net cost to fitness in the progeny arising from population mixtures) really exist? If it does exist, in what sorts of species can we expect to observe it? How does it relate to physical distance between populations and to species’ intrinsic dispersal capabilities, and can we expect the initial effects of outbreeding depression to decline during the generations following a translocation event?