Long-term, fine-scale temporal patterns of genetic diversity in the restored Mauritius parakeet reveal genetic impacts of management and associated demographic effects on reintroduction programmes
Introduction
Reintroductions, translocations and reinforcements (IUCN, 1998, Seddon et al., 2012) are techniques frequently used in the conservation of endangered species to re-establish populations within their historic range (Griffith et al., 1989, IUCN, 1998, Seddon, 1999). However, the success of such projects has been variable and many have failed (Armstrong and Seddon, 2008, BECK et al., 1994). A multitude of putative reasons for failure have been put forward and include issues associated with inbreeding in small populations and the outbreak of disease, factors which may go undetected in unsuccessful reintroduction attempts due to inadequate post-release monitoring and failure to identify a priori targets concerned with assessing success (Fischer and Lindenmayer, 2000, Nichols and Williams, 2006, Seddon et al., 2007). The existence of long-term datasets concerning successfully reintroduced populations which have been closely monitored can therefore be of great value for evaluating management strategies aiming to maximise reintroduction success. These data can provide the opportunity to examine detailed temporal changes in genetic diversity, population structure and levels of inbreeding, variables which are assumed to be important parameters in reintroduction success and population recovery (Groombridge et al., 2012, Keller et al., 2012). Such threatened populations often exist in fragmented landscapes consisting of small, isolated pockets of individuals with limited dispersal, thereby further increasing spatial associations between relatives and ultimately resulting in fine-scale genetic structure among population fragments (Slatkin, 1987, Beck et al., 2008, Randall et al., 2010).
The primary aim of most species recovery programmes is to increase population sizes from very low numbers. The genetic consequences of these recoveries, including increased levels of inbreeding and reduced genetic diversity due to random drift (Groombridge et al., 2000, Keller et al., 2001, Jamieson, 2011), are often overlooked as secondary considerations among wildlife managers (Frankham, 2010). Reintroducing and translocating individuals does not necessarily guarantee that the insidious effects of drift and subpopulation isolation are mitigated and retrospective assessments of conservation actions, combined with population simulations which consider multiple scenarios, can provide managers with the information required to maximise population viability by minimising detrimental genetic effects. Only studies of long-term, fine-scale genetic patterns of wild populations can provide this level of detailed information and few examples from threatened species exist which incorporate comprehensive, molecular data of breeding individuals collected over several generations (Wisely et al., 2002, Jamieson et al., 2006, Vonholdt et al., 2010, Brekke et al., 2011).
Evaluating the genetic effects of conservation management has important implications for future reintroduction and recovery attempts. By applying a fine-scale approach to monitor levels of genetic diversity, the effects of different management techniques (Nussey et al., 2005) or stochastic events such as disease outbreaks (Randall et al., 2010) can be assessed relative to the viability and reproductive success of the threatened population. This approach can provide managers with an adaptive framework with which to manage threatened species and improve the chances of success for future reintroduction programmes by focusing on: (i) the rates of change in levels of genetic diversity at both the population and subpopulation level, (ii) the genetic effects of population augmentation through reintroduction or translocation, (iii) the extent to which inbreeding and genetic factors might influence recruitment and survival, and (iv) the genetic implications of intensive conservation management. Intuitively, the transfer of individuals between multiple managed populations in the form of translocations and, reintroductions, which commonly form part of intensive conservation management activities, can be expected to promote gene flow and genetic homogenisation, and consequently limit the loss of population genetic diversity via drift. However, establishing whether or not such benefits have actually occurred is seldom common practice amongst species conservation and monitoring programmes but is important for directing future long-term management.
Addressing these genetic considerations requires long-term genetic sampling combined with detailed individual-level life-history data that can only be found in long-term and intensive conservation management programmes. One such example involves the successful recovery of the Mauritius (or echo) parakeet (Psittacula echo), an endangered species which has, as a consequence of a sustained field monitoring effort spanning two decades, been documented in unprecedented detail. Intensive conservation intervention has recovered this species from an estimated population size of fewer than 20 individuals in the 1980s (Jones and Duffy, 1993) to more than 500 in 2011 (MWF, 1994–2012). Additionally, this long-term management has resulted in a genotype dataset of over 900 individuals and the existence of an extensive social pedigree incorporating life history data for over 1100 individuals since the early 1990s. By incorporating these detailed genetic datasets and information regarding historical management strategies with appropriate demographic and population genetic simulation software it is possible to evaluate how well existing management practices perform at achieving predetermined goals associated with maximising population genetic viability. The conservation programme for the Mauritius parakeet therefore provides an ideal opportunity to examine in detail patterns of temporal and spatial genetic processes associated with the recovery of a threatened species re-established via reintroductions into a fragmented landscape.
In this study, we use fine-scale, spatio-temporal analyses as a monitoring tool to elucidate patterns of population genetic variation in a recovering, bottlenecked and managed parakeet species spanning the 16-year recovery period since intensive management began. Detailed population monitoring records combined with molecular data offer an insight into the genetic consequences of managed translocations and reintroductions of this species. Incorporating population viability software with this kind of empirical data provides a powerful tool with which to derive forward simulations of population genetic processes under different scenarios which can be crucial to informing future management decisions. Importantly, long-term studies such as this provide the data necessary to ground-truth such simulations. Here we provide recommendations for future management strategies based upon empirical evidence and simulated scenarios using a fine-scale, year-to-year resolution of genetic data. In doing so, we reveal precise genetic effects of management, the lessons from which are applicable to many conservation projects.
Section snippets
Study system
The Mauritius parakeet is estimated to have diverged during the late Miocene/Pliocene from the ringneck (P. krameri) parakeets where it appears to have colonised Mauritius during the radiation of ringnecks across India and Africa (Groombridge et al., 2004, Kundu et al., 2011) and represents the only remaining Psittacula species native to the Western Indian Ocean. Previous work suggests that this species has maintained relatively high levels of genetic diversity (Taylor and Parkin, 2010) despite
Genotyping
A total of 897 individuals were genotyped spanning a maximum of five generations from 1993 to 2011. Genotyping error rates were less than 0.5% and the estimated frequencies of null alleles per locus were less than 0.1% for all loci. A total of 109 alleles were identified across the entire dataset; average number of alleles per locus ranged from 4 to 10.8 (mean: 6.8 ± 1.87) and average expected heterozygosity ranged from 0.27 to 0.81 (mean 0.64 ± 0.04). Results of tests for linkage disequilibrium
Metapopulation levels of genetic diversity
Our results support conclusions from previous work (Taylor and Parkin, 2010) that this species appears to have retained relatively high levels of heterozygosity despite an apparent population bottleneck. Assuming that as an island endemic species, the population (and thus genetic diversity) has always been restricted relative to continental species (Frankham, 2002), this observation is somewhat surprising. A level of heterozygosity of 10% was recorded for the restored population of the endemic
Conclusions
Rapidly declining species often require intervention that demands an immediate focus on boosting numbers of individuals, where considerations of genetic factors are of secondary importance to the more immediate threat of extinction caused by habitat destruction or introduced predators. Post-recovery genetic analysis of such species recoveries is often concerned with quantifying the loss of genetic diversity of species at the metapopulation level as a result of population bottlenecks, which
Acknowledgements
This work was funded by a NERC CASE PhD studentship award to JG in partnership with Wildlife Vets International. Genotyping was performed at the NERC Biomolecular Analysis Facility supported by the Natural Environment Research Council, UK. We would like to thank Andy Krupa for laboratory assistance, the National Parks and Conservation Service of the Government of Mauritius and all the staff and volunteers at the Mauritius Wildlife Foundation for their assistance in sample collection and
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