Biological Conservation 142 (2009) 2915–2922 Contents lists available at ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon Captive breeding genetics and reintroduction success Alexandre Robert * UMR 7204 MNHN-CNRS-UPMC, Conservation des Espèces, Restauration et Suivi des Populations, Muséum National d’Histoire Naturelle, CRBPO, 55, Rue Buffon, 75005 Paris, France article info abstract Article history: Since threatened species are generally incapable of surviving in their current, altered natural environ- Received 6 May 2009 ments, many conservation programs require to preserve them through ex situ conservation techniques Received in revised form 8 July 2009 prior to their reintroduction into the wild. Captive breeding provides species with a benign and stable Accepted 23 July 2009 environment but has the side effect to induce significant evolutionary changes in ways that compromise Available online 26 August 2009 fitness in natural environments. I developed a model integrating both demographic and genetic processes to simulate a captive-wild population system. The model was used to examine the effect of the relaxation Keywords: of selection in captivity on the viability of the reintroduced population, in interaction with the reintro- Reintroduction duction method and various species characteristics. Results indicate that the duration of the reintroduc- Selection relaxation Population viability analysis tion project (i.e., time from the foundation of the captive population to the last release event) is the most Mutational meltdown important determinant of reintroduction success. Success is generally maximized for intermediate project duration allowing to release a sufficient number of individuals, while maintaining the number of generations of relaxed selection to an acceptable level. In cases where a long residence time in captivity cannot be avoided, the use of distinct, genetically independent captive breeding units allows more effi- cient purging of the genetic load in the reintroduced population, and substantially improves its viability. Overall, the study allows to identify situations in which the genetic cost associated with selection relax- ation may overwhelm the demographic benefits of programs. Ó 2009 Elsevier Ltd. All rights reserved. 1. Introduction important to assess their viability after a sufficiently long time. This can be achieved easily with population dynamics models, The reintroduction of plants and animals to the wild is an which allow computing and comparing long-term extinction rates important technique to save endangered species from extinction for various situations or release methods. For animal species, gen- (Armstrong and Seddon, 2008). Since rare species are generally eral empirical surveys on reintroduction success have concluded incapable of surviving in their current, altered natural environ- that success is generally low (38%, Griffith et al., 1989; 11%, Beck ments, many conservation programs are required to preserve them et al., 1994) and that reintroduction projects using captive-bred through ex situ conservation techniques (captive breeding, zoos, animals were significantly less successful than those using wild aquaria, arboreta, gene and seed banks) before the reintroduction animals (Griffith et al., 1989; Wolf et al., 1996; Fischer and Linden- phase can be achieved. The success of reintroduction programs is mayer, 2000; Jule et al., 2008). difficult to assess because such assessment requires long term data Ex situ techniques provide species with a benign and stable as well as general and accepted success criteria, which are both environment (through e.g., food supplementation, health care, lacking. In most empirical surveys on reintroductions, programs reduction of parasite and disease loads, removal of predators) in are considered successful if they result in self-sustaining popula- order to ensure high and temporally stable population growth tions (Griffith et al., 1989; Fischer and Lindenmayer, 2000). While and high probability of long term persistence. Although captivity failures are easy to identify in some cases (e.g., when extinction is may cause physiological, behavioral or ecological problems, empir- documented), the assessment of successes may require the use of ical results in various species indicate that fecundity and survival various criteria (survival or fecundity rates, population trend, spa- rates are generally higher in captive than in wild populations tial expansion...) to determine whether or not the population is (e.g., Ricklefs and Scheurlein, 2001). In Salmonids, for instance, sur- self-sustaining. Because reintroduced populations are generally vival from egg to smolt stages is typically 85–95% in hatcheries but small and may exhibit a demographic disequilibrium (e.g., in terms only 1–5% in the wild (Reisenbichler et al., 2004). of sex or age structure) affecting their short-term dynamics, it is The cost of this demographic security is that captive popula- tions may undergo significant evolutionary changes in ways that * Tel.: +33 1 40 79 57 27; fax: +33 1 40 79 38 35. compromise fitness in natural, non benign environments (Ruzzan- E-mail address: [email protected] te and Doyle, 1993). There are many empirically documented 0006-3207/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2009.07.016 2916 A. Robert / Biological Conservation 142 (2009) 2915–2922 examples of reductions in fitness caused by captive propagation populations were considered, assuming that selection against del- (Fleming et al., 1996; Bryant and Reed, 1999; Lomnicki and Jasien- eterious alleles was relaxed in captivity. Projected long-term ski, 2000) and recent results indicate that the reduction of repro- extinction probabilities were computed as an index of reintroduc- ductive capabilities in the wild can be as fast and as strong as tion success. 40% decline per captive-reared generation (Araki et al., 2007). Depending on the captive conditions, populations may face dif- 2. Methods ferent types of genetic problems in captivity: (i) a high level of inbreeding due to small population size, and the resulting reduc- I used a two-sex individual-based model with overlapping gen- tion of fitness due to inbreeding depression (Ralls et al., 1988); erations and a yearly time step to describe the dynamics of a sys- (ii) the progressive fixation and accumulation of mildly deleterious tem of captive (one or several breeding units) and reintroduced mutations through genetic drift (Bryant and Reed, 1999); (iii) the (single, initially empty site) populations. These two components loss of genetic diversity (Neveu et al., 1998), (iv) genetic adapta- are hereafter referred to as the captive and the wild populations. tions to captivity that are deleterious in the wild (Frankham, 2008). Importantly, these different problems may be either associ- 2.1. Life cycle and dynamics of the wild population ated with small population size, captive benign conditions, artifi- cial selection, or their interactions. In each year t, adult males and females paired randomly accord- As a consequence of this variety of ecological and evolutionary ing to a monogamous mating system. The female fecundity was F(t) processes, optimal management strategies for restored populations (Poisson process) and the sex of each individual was randomly are dependent on the goal and focus of the programs. First, man- determined according to a 1:1 sex-ratio. Each survival event was agement strategies that are optimal for the wild population may drawn from a Bernoulli function, with age-specific survival rates. be the ones that are the most detrimental to the captive one, for Because the type of density dependence had little effect on extinc- demographic (Bustamante, 1996) and genetic (Earnhardt, 1999) tion rates for the questions investigated and at the time scale con- reasons. Second, in the captive population, there may be genetic sidered, population size was simply truncated to the population’s trade-offs among breeding strategies (e.g., strategies aiming at carrying capacity Kwild in each year. Truncation was made indepen- maximizing the genetic diversity of the captive populations by dently of the genetic qualities of individuals in order to keep con- equalization of individual contributions may enhance selection stant selection coefficients. For simplicity, I assumed that relaxation (but see Rodriguez-Ramilo et al., 2006)). Third, strate- environmental stochasticity caused inter-annual variations in gies that are demographically optimal may be the ones that are fecundity, but not in survival. In each year t, the value of F(t) was likely to be the most genetically deleterious (Lynch and O’Hely, drawn from a Normal distribution (F, rF). The theoretical set of 2001). demographic parameters used in the main simulation corresponds Theoretical modeling work on the optimal management of cap- to typical short-lived birds or mammals, with low annual adult sur- tive-wild population systems has shown contrasting results, which vival rates (sad < 0.7) and high annual fecundity rates (F > 4) (param- reflect the diversity of evolutionary and ecological processes in- eters used are presented in Table 1). However, to examine the volved, as well as their antagonisms. From a purely demographic generality of the conclusions, I investigated other types of life cycles view-point (i.e., in the absence of genetic considerations), model- (corresponding, in particular, to long-lived vertebrates). The demo- ing work