Response to comment on “Individual heterozygosity predicts translocation success in endangered desert turtles”

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Abstract

Hansson et al. argue that our main finding could provide a metric that is too simplistic to maximize genetic rescue. They agree that translocation of the most genetically diverse individuals has led to a large increase in the survival of translocated turtles, but instead recommend relocating individuals that have a low genetic load and the greatest representation of metapopulation diversity. Their recommendation is based on specific model assumptions and fitness effects which are often unknown and not generalizable to many endangered species applications.

Scott et al. (1) showed that individual heterozygosity, but not the original genetic clade or geographic distance, correlated with post-translocation survival in Mojave Desert turtles. With this main finding, we argued that individual heterozygosity is an important tool that conservation biologists could use to determine which individuals to transfer. Hansson et al. (2) argue that this recommendation could be wrong as it ignores the potential increase in gene load that could follow post-translocation reproduction. They argue that translocation from less heterozygous individuals who have been purged of the deleterious variation would be a safer approach, and they provide simulation data to support their argument. Hansson et alCriticism of. may be reasonable for some specific cases of genetic rescue, but they are unlikely to be generalizable, nor do they negate our results. Here, we argue that our conclusion is always important when planning transfers, and we reiterate Scott’s conclusion. et al. that many ecological and genetic factors must be taken into account in transfer programs. We maintain our main conclusion: for translocations to be successful, individuals must survive, and more heterozygous individuals have higher survival. The additional benefits to the population in later generations are important, but the survival of transferred individuals must take place first, and for most species, survival after transfer is the most lethal part of the transfer process (36).

Hansson et al. imply that we recommend individual heterozygosity as the sole or primary consideration when translocating individuals, which we do not. They then build on the sometimes controversial but long-standing tradition of modeling that uses simulations and population genetics theory to determine the optimal source population (s) to use to facilitate genetic rescue (7). In a specific set of conditions for population differentiation, Hansson et al. show that translocation of the 20% of individuals with the greatest genetic diversity can have two main effects: (i) If there is a lot of genetic structure in a species, then one can end up transferring only a subset of the total genetics at the level of the species diversity, because these 20% can come exclusively from one or a few demes; and (ii) the choice of this set of individuals may increase the genetic load in subsequent generations compared to other translocated selection scenarios. These results can be true in an idealized situation. However, they do not reflect the reality or the purposes of the turtle translocations we studied. Hansson et al. model a specific partition of genetic variation within and between demes, and they suggest that by selecting only the most diverse individuals overall, some demes will not have enough heterozygous individuals to be translocated, thus resulting in a loss of diversity between demes. If this diversity among demes is related to fitness, either of the translocated individuals or their offspring, then an important component of the genetic variation is potentially lost. All of this may or may not be true, and it almost certainly varies across case studies. In the Mojave Desert tortoise, there are two major genetic groups (north and south) and a strong component of distance isolation within each. We show that there is no difference in the translocated geographic distance or the genetic population of origin between the individuals who lived or perished after the translocation. [figures 2 and 3 of (1)]. There is some uncertainty (about 36 km on average) on the site of origin of the displaced turtles, but this should not be biased by the status of the turtle; therefore, there is no reason why Hansson et alThe suggestion of. that there is “substantial noise” in our alleged turtle origins would alter our main conclusion. Only individual heterozygosity made the difference.

As we originally pointed out (1), there are many potential goals motivating translocations, including repatriation of displaced individuals, population supplementation / recovery, facilitation of the flow of adaptive variation, and genetic rescue. The potential for increased gene load may or may not be first-rate given these goals and situations. Given the near impossibility of accurately estimating the fitness consequences of individual substitutions across the genome, we doubt that empirical studies are able to simultaneously model the joint positive effects of heterozygosity on survival and the effects of heterozygosity. negatives of different allelic combinations after breeding in systems most important for conservation. Although models such as Genomic Evolution Rate Profiling (GERP) (8) can be used to estimate the potential genomic load from genomic signatures, these models are at best an approximation of the load. In addition, there appears to be little correlation between neutral genetic variation at the genome level and inbreeding depression, genetic load, or adaptive potential (9); thus, you really have to understand the individual loci for the load argument to be effective. Therefore, in situations where reducing gene load during gene rescue is a priority for translocation-based conservation measures, we recommend that the specific genetic condition of donor and source populations be investigated (ten) rather than following more generalized rules based on maximizing genetic diversity or minimizing the genetic load of the source population (s).

Hansson et al. also argue that we have oversimplified the basic operational practice of avoiding moving individuals long distances or across population boundaries. We do not agree. When other detailed information is lacking, minimizing distance or interclade translocation is literally the guiding principle of the manual (11). For Mojave Desert turtles, explicit recommendations based on geographic distance (12) or genetic clade (13) were the guiding principles (14). However, at least at the large-scale translocation site, where the main goals were to re-invade displaced or abandoned turtles and gain a better understanding of the factors underlying translocation survival, the end result was that most turtles died. Anything that can reverse this potentially devastating outcome is significant. When undertaking translocations for management, there are a variety of considerations, including environmental mismatch, phenology, behavior, season and genetics, all of which come into play. Our work indicates that individual genetic diversity should be included as a measure that can be used to improve post-translocation survival. It certainly appears to be important in desert turtles.

We applaud Hansson et alThe concern and the simulation work of. aimed to understand and minimize the potential future genetic load that could arise from translocation events. Further, we agree that if the fitness consequences of each mutation were known, individuals purged of deleterious mutations existed, and it could be ensured that they would live to reproduce, we might be able to increase the overall efficiency of translocations and genetic rescue. However, these models simplify the very complex real-world conservation needs and are probably not currently applicable to most non-model systems, especially given the difficulty of accurately estimating gene load. We stand by our initial conclusion that high individual heterozygosity improved translocation survival, and hope this becomes one more measure conservation biologists continue to test and consider in the ever-growing toolbox. available to conservation managers.

The references

  1. R. Frankham et al., Genetic management of fragmented animal and plant populations (Oxford Univ. Press, 2017).

  2. United States Fish and Wildlife Service, Translocation of Mojave Desert Turtles from Project Sites: Guidelines for Plan Development (2020).



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