The inflated significance of neutral genetic diversity in conservation genetics

Teixeira, João C.; Huber, Christian D.

doi:10.1073/pnas.2015096118

Cited by 322 publications

(297 citation statements)

References 166 publications

(239 reference statements)

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“…The first alleged problem with the use of genetic diversity in conservation is the lack of supporting evidence for the idea that higher levels of genetic diversity lead to an increase in fitness and long‐term survival with a concomitant reduction in species extinction risk. Indeed, Teixeira and Huber (2021) write that “no simple general relationship exists between neutral genetic diversity and the risk of species extinction.” Notwithstanding the paradoxical view of neutrality, such sweeping statements mischaracterize an impressive literature that spans decades. Textbook examples of the positive relationship between genetic diversity and fitness abound, including examples in fruit flies ( Drosophila melanogaster ) (Frankham, 1995), monkeyflower ( Mimulus guttatus ) (Willis, 1993) and field mice ( Peromyscus leucopus ) (Lacy et al, 2013), as well as many other diverse organisms that occupy a variety of ecosystems (Table 1; see also Chapman et al, 2009; Hedrick & Kalinowski, 2000).…”

Section: Species Ecosystem Gd Marker Gd Estimator Referencementioning

confidence: 99%

“…The fourth point used to dismiss the usefulness of conserving genetic diversity is that to do so requires a better understanding of functional genetic diversity, demographic history and ecological relationships for conservation (Teixeira & Huber, 2021). We think this is a straw man; one would be hard pressed to find a respectable conservation geneticist who thought otherwise.…”

Section: Species Ecosystem Gd Marker Gd Estimator Referencementioning

confidence: 99%

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The long‐standing significance of genetic diversity in conservation

et al. 2021

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Since allozymes were first used to assess genetic diversity in the 1960s and 1970s, biologists have attempted to characterize gene pools and conserve the diversity observed in domestic crops, livestock, zoos and (more recently) natural populations. Recently, some authors have claimed that the importance of genetic diversity in conservation biology has been greatly overstated. Here, we argue that a voluminous literature indicates otherwise. We address four main points made by detractors of genetic diversity's role in conservation by using published literature to firmly establish that genetic diversity is intimately tied to evolutionary fitness, and that the associated demographic consequences are of paramount importance to many conservation efforts. We think that responsible management in the Anthropocene should, whenever possible, include the conservation of ecosystems, communities, populations and individuals, and their underlying genetic diversity.

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Section: Species Ecosystem Gd Marker Gd Estimator Referencementioning

confidence: 99%

Section: Species Ecosystem Gd Marker Gd Estimator Referencementioning

confidence: 99%

The long‐standing significance of genetic diversity in conservation

et al. 2021

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“…It has been proposed that the increase of extinction risk ascribed to the deleterious alleles introduced during genetic rescue can be controlled by prioritizing a lower putative load inferred from genomic analysis over a high genetic diversity (Kyriazis et al 2020; Teixeira and Huber 2021). However, relying on the ability to identify the mutations that are responsible for a main fraction of the fitness load is not free of perils (Kardos and Shafer 2018; Ralls et al 2020; García-Dorado and Caballero 2021).…”

Section: Some Background On Purging and On Its Role During Genetic Rescuementioning

confidence: 99%

Reviewing the consequences of genetic purging on the success of rescue programs

Pérez‐Pereira

Caballero

García-Dorado

2021

Preprint

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Genetic rescue is increasingly considered a promising and underused conservation strategy to reduce inbreeding depression and restore genetic diversity in endangered populations, but the empirical evidence supporting its application is limited to a few generations. Here we discuss on the light of theory the role of inbreeding depression arising from partially recessive deleterious mutations and of genetic purging as main determinants of the medium to long-term success of rescue programs. This role depends on two main predictions: (1) The inbreeding load hidden in populations with a long stable demography increases with the effective population size; and (2) After a population shrinks, purging tends to remove its (partially) recessive deleterious alleles, a process that is slower but more efficient for large populations than for small ones. We also carry out computer simulations to investigate the impact of genetic purging on the medium to long term success of genetic rescue programs. For some scenarios, it is found that hybrid vigor followed by purging will lead to sustained successful rescue. However, there may be specific situations where the recipient population is so small that it cannot purge the inbreeding load introduced by migrants, which would lead to increased fitness inbreeding depression and extinction risk in the medium to long term. In such cases, the risk is expected to be higher if migrants came from a large non-purged population with high inbreeding load, particularly after the accumulation of the stochastic effects ascribed to repeated occasional migration events. Therefore, under the specific deleterious recessive mutation model considered, we conclude that additional caution should be taken in rescue programs. Unless the endangered population harbors some distinctive genetic singularity whose conservation is a main concern, restoration by continuous stable gene flow should be considered, whenever feasible, as it reduces the extinction risk compared to repeated occasional migration and can also allow recolonization events.

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“…Ex situ sampling designs traditionally rely on neutral population genetic structure to guide sampling decisions (Caujapé-Castells & Pedrola-Monfort, 2004; Gapare, Yanchuk, & Aitken, 2008; Hoban, 2019; Hoban & Schlarbaum, 2014). However, concerns exist regarding the sole use of neutral genetic variability for species conservation, as variation at neutral loci is unlikely to reflect adaptive genetic diversity (Bonin, Nicole, Pompanon, Miaud, & Taberlet, 2007; Holderegger, Kamm, & Gugerli, 2006; McKay & Latta, 2002; Teixeira & Huber, 2021). Ex situ population sampling may need to evaluate the impact different evolutionary processes have had on population genetic structure to optimize neutral and adaptive variation collected.…”

Section: Introductionmentioning

confidence: 99%

Reduced representation sequencing to understand the evolutionary history of Torrey pine (Pinus torreyana Parry) with implications for rare species conservation

Santo

Hoban

Parchman

et al. 2021

Preprint

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Understanding the contribution of neutral and adaptive evolutionary processes to population differences is often necessary for better informed management and conservation of rare species. In this study, we focused on Pinus torreyana Parry (Torrey pine), one of the world's rarest pines, endemic to one island and one mainland population in California. Small population size, low genetic diversity, and susceptibility to abiotic and biotic stresses suggest Torrey pine may benefit from inter-population genetic rescue to preserve the species' evolutionary potential. We leveraged reduced representation sequencing to tease apart the respective contributions of stochastic and deterministic evolutionary processes to population differentiation. We applied these data to model spatial and temporal demographic changes in effective population sizes and genetic connectivity, to assess loci possibly under selection, and evaluate genetic rescue as a potential conservation strategy. Overall, we observed exceedingly low standing variation reflecting consistently low effective population sizes across time and limited genetic differentiation suggesting maintenance of gene flow following divergence. However, genome scans identified more than 2000 SNPs candidates for divergent selection. Combined with previous observations indicating population phenotypic differentiation, this indicates that natural selection has likely contributed to population genetic differences. Thus, while reduced genetic diversity, small effective population size, and genetic connectivity between populations suggest genetic rescue could mitigate the adverse effect of rarity, divergent selection between populations indicates that genetic mixing could disrupt adaptation. Further work evaluating the fitness consequences of inter-population admixture is necessary to empirically evaluate the trade-offs associated with genetic rescue in Torrey pine.

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The inflated significance of neutral genetic diversity in conservation genetics

Cited by 322 publications

References 166 publications

The long‐standing significance of genetic diversity in conservation

The long‐standing significance of genetic diversity in conservation

Reviewing the consequences of genetic purging on the success of rescue programs

Reduced representation sequencing to understand the evolutionary history of Torrey pine (Pinus torreyana Parry) with implications for rare species conservation

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