Predicting and prioritizing genetic diversity outcomes of animal translocations

Environmental change is driving extinctions and isolating species globally; recovering and rescuing these populations has motivated conservation for over a century (Seddon et al., 2014). Traditionally, recovery to selfsustaining populations have focused on habitat management approaches that ultimately increase the survival and reproduction of the at-risk population. However, genetic diversity is increasingly recognized as an integral component of long-term species recovery from past changes and to provide adaptive capacity to future change (Jamieson & Lacy, 2012). Indeed, population declines, and isolation has reduced genetic diversity and increased inbreeding that escalates the extinction risk for threatened species (Forester et al., 2022). Translocations, or the intentional movement of animals to repatriate extirpated or augment existing populations, have become a central tool for species recovery. Increasingly, translocations are viewed not only to bolster population size, but also genetic diversity. Indeed, translocations can improve fitness through the introduction of new genetic material when the recipient population is small or inbred and improve adaptive potential by increasing genetic diversity (Weeks et al., 2011; Whiteley et al., 2015). While increasing genetic diversity is often cited as a fundamental goal of translocations, the effectiveness is often not evaluated (but see Jackson et al., 2022). Improving genetic diversity hinges on selecting an appropriate source population and identifying the correct number of individuals to be translocated; conservation practitioners, though, rarely have prior knowledge on the genetics of translocated individuals to inform either condition (Tracy et al., 2011). Even when known, the persistence of genetic diversity in the recipient population is often unexplored. By combining genetic data on the source with simulations to predict the rate of genetic loss, practitioners can improve both planning and outcomes of translocations for the maintenance of genetic diversity (Grueber et al., 2019; Weiser et al., 2013). Herein, we quantified the genetic diversity of translocated individuals, and then simulated how genetic diversity would erode over time Received: 20 September 2022 Revised: 8 March 2023 Accepted: 3 April 2023


| THE PROBLEM
Environmental change is driving extinctions and isolating species globally; recovering and rescuing these populations has motivated conservation for over a century (Seddon et al., 2014). Traditionally, recovery to selfsustaining populations have focused on habitat management approaches that ultimately increase the survival and reproduction of the at-risk population. However, genetic diversity is increasingly recognized as an integral component of long-term species recovery from past changes and to provide adaptive capacity to future change (Jamieson & Lacy, 2012). Indeed, population declines, and isolation has reduced genetic diversity and increased inbreeding that escalates the extinction risk for threatened species (Forester et al., 2022).
Translocations, or the intentional movement of animals to repatriate extirpated or augment existing populations, have become a central tool for species recovery. Increasingly, translocations are viewed not only to bolster population size, but also genetic diversity. Indeed, translocations can improve fitness through the introduction of new genetic material when the recipient population is small or inbred and improve adaptive potential by increasing genetic diversity (Weeks et al., 2011;Whiteley et al., 2015). While increasing genetic diversity is often cited as a fundamental goal of translocations, the effectiveness is often not evaluated (but see Jackson et al., 2022).
Improving genetic diversity hinges on selecting an appropriate source population and identifying the correct number of individuals to be translocated; conservation practitioners, though, rarely have prior knowledge on the genetics of translocated individuals to inform either condition (Tracy et al., 2011). Even when known, the persistence of genetic diversity in the recipient population is often unexplored. By combining genetic data on the source with simulations to predict the rate of genetic loss, practitioners can improve both planning and outcomes of translocations for the maintenance of genetic diversity (Grueber et al., 2019;Weiser et al., 2013). Herein, we quantified the genetic diversity of translocated individuals, and then simulated how genetic diversity would erode over time under different scenarios: single translocation, additional augmentations, and rates of natural immigration.

| CASE STUDY
Throughout their distributional range in the Great Lakes Region, Sharp-tailed grouse (Tympanuchus phasianellus) are declining in abundance and increasingly isolated. Small population sizes and limited gene flow put sharptailed grouse populations at increased risk of local extirpation. To mediate declines, a federal, state, and tribal partnership has begun to restore critical habitat and augment the contemporary population on the Moquah Barrens Wildlife Management Area in northwestern Wisconsin ( Figure S1). Concomitant with these goals was also the objective of increasing genetic diversity.
Over 3 years, 160 sharp-tailed grouse were translocated from a neighboring, but disjunct population in northwestern Minnesota. This source population exhibits high-genetic diversity, making it an ideal source for the translocation (Roy & Gregory, 2019). However, debate exists between minimizing the presence of strongly deleterious alleles (Kyriazis et al., 2021) or maximizing diversity of source populations (Ralls et al., 2020). Nevertheless, the general recommendation of choosing a source population that maximizes genetic diversity is well supported by empirical evidence and history of past augmentation outcomes (Frankham, 2015). Indeed, observed heterozygosity and number of alleles were similar between the source and translocated populations (Appendix S1). Simulations revealed that the genetic diversity, measured as retention of rare alleles (Weiser, Grueber, & Jamieson, 2012), of the recipient population would erode rapidly if no further management actions were taken (Figure 1a; Appendix S1). Augmentations at 10-or 25-year frequency increased the retention of genetic diversity but also eventually eroded due to small population size (Figure 1a). However, only four migrants per year was enough to retain rare alleles (Figure 1b). Increased connectivity was necessary to maintain genetic diversity and translocations alone, even at relatively high frequency, were subject to genetic loss without consistent natural immigration.

| DISCUSSION
Despite successful selection and release of translocated individuals, follow-up monitoring is essential to evaluate whether the diversity captured in the translocated population is incorporated into the extant population. Indeed, our findings show that the initial increase of genetic F I G U R E 1 Simulated probability of retaining rare alleles (q = 0.05) following a translocation of sharp-tailed grouse (Tympanuchus phasianellus) to northern Wisconsin under different augmentation strategies (a) and dependent on the number of migrants per year (b). Image of sharp-tailed grouse wearing a VHF transmitter after translocation to monitor movement, survival, and habitat use (c). diversity quickly eroded with no further action and is likely common for many at-risk species (Jackson et al., 2022). Importantly, these simulations provide a reference and target for restoration efforts and increasing connectivity would minimize the frequency and intensity of additional augmentations and should be adopted more broadly in the planning and management of at-risk populations. For such isolated and small populations, which are typical for translocations not just here but elsewhere, future augmentations and maintaining connectivity through the planning of a recovery network (i.e., a natural metapopulations but emerging from human agency; Smith et al., 2021) is critical to meet the stated goals of increasing genetic diversity and population persistence. This case study highlights the importance of a priori assessment of the genetic makeup of translocated individuals and number to release as well as the erosion of genetic diversity to plan future augmentations and identify thresholds for connectivity.
While demographic monitoring post translocation is often emphasized in management plans and is important for short-term persistence (Figure 1c), genetic diversity will play an important role in long-term persistence. With the increasing application of genomics in conservation, new opportunities are emerging to better assess the genetic benefits and risk from translocations and will be integral in future designs to evaluate sources and evolutionary potential among populations (Forester et al., 2022). In general, conservation practitioners can promote genetic diversity of translocations by (1) Sourcing individuals from a genetically diverse population; (2) Releasing a sufficient number that captures the genetic diversity of the source population; (3) Choosing a reintroduction site with connectivity to neighboring populations in the attempt to create a recovery network; (4) Evaluating the loss of genetic diversity through simulations to guide management plans; (5) Monitoring for genetic diversity following translocation. Translocations are essential tools to mediate the effects of environmental change and conservation practitioners should explicitly incorporate genetic diversity into management plans and evaluate alternative strategies, and ultimately adapt strategies following monitoring that promote the long-term persistence of genetic diversity.

ACKNOWLEDGMENTS
This work was supported by the Great lakes Restoration Initiative and the United States Department of Agriculture Joint Chiefs Initiative through partnership with the Wisconsin Sharp-tailed Grouse Society and United States Forest Service. We thank partners that provided expertise and logistical support: Wisconsin Department of Natural Resources, Bad River Band of Lake Superior Chippewa, Red Cliff Band of Lake Superior Chippewa, Great Lakes Indian Fish and Wildlife Commission, Minnesota Department of Natural Resources, Minnesota Sharptailed Grouse Society, US Fish and Wildlife Service, and the Nature Conservancy. A special thanks to Bill Berg, Tom Doolittle, Dave Evenson, Jim Evrard, Aaron Fahlstrom, Ruth Anne Frank, Bob Hanson, Dr. Lisa Jeanetta DVM, Heather Jensen, Greg Kessler, Alexandra Lehner, Todd Naas, Jim Nissen, Jodie Provost, Charlotte Roy.