Journal of Heredity, 2022, 113, 491–499
https://doi.org/10.1093/jhered/esac037
Advance access publication 5 August 2022
Original Article
Received January 19, 2022; Accepted August 2, 2022
Original Article
Give and Take: Effects of Genetic Admixture on Mutation
Load in Endangered Florida Panthers
Alexander Ochoa
1,
, David P. Onorato
2,
, Melody E. Roelke-Parker
3,
, Melanie Culver
4,
,
Robert R. Fitak
1,
1
Department of Biology and Genomics and Bioinformatics Cluster, University of Central Florida, Orlando, FL 32816, USA,
2
Fish and Wildlife Research Institute, Florida Fish and Wildlife Conservation Commission, Naples, FL 34114, USA,
3
Frederick National Laboratory for Cancer Research, Leidos Biomedical Research, Inc., Fredrick, MD 21701, USA,
4
U.S. Geological Survey, Arizona Cooperative Fish and Wildlife Research Unit, and School of Natural Resources and the Environment, University
of Arizona, Tucson, AZ 85721, USA
Address correpondence to A. Ochoa at the address above, or e-mail: alexander.ochoa@ucf.edu.
Corresponding Editor: Klaus-Peter Koepfi
Abstract
Genetic admixture is a biological event inherent to genetic rescue programs aimed at the long-term conservation of endangered wildlife. Although
the success of such programs can be measured by the increase in genetic diversity and fitness of subsequent admixed individuals, predictions
supporting admixture costs to fitness due to the introduction of novel deleterious alleles are necessary. Here, we analyzed nonsynonymous
variation from conserved genes to quantify and compare levels of mutation load (i.e. proportion of deleterious alleles and genotypes carrying
these alleles) among endangered Florida panthers and non-endangered Texas pumas. Specifically, we used canonical (i.e. non-admixed) Florida
panthers, Texas pumas, and F
1
(canonical Florida × Texas) panthers dating from a genetic rescue program and Everglades National Park panthers
with Central American ancestry resulting from an earlier admixture event. We found neither genetic drift nor selection significantly reduced
overall proportions of deleterious alleles in the severely bottlenecked canonical Florida panthers. Nevertheless, the deleterious alleles identified
were distributed into a disproportionately high number of homozygous genotypes due to close inbreeding in this group. Conversely, admixed
Florida panthers (either with Texas or Central American ancestry) presented reduced levels of homozygous genotypes carrying deleterious
alleles but increased levels of heterozygous genotypes carrying these variants relative to canonical Florida panthers. Although admixture is likely
to alleviate the load of standing deleterious variation present in homozygous genotypes, our results suggest that introduced novel deleterious
alleles (temporarily present in heterozygous state) in genetically rescued populations could potentially be expressed in subsequent generations
if their effective sizes remain small.
Key words: deleterious variation, genetic drift, genetic rescue, inbreeding, small populations, wildlife conservation
Introduction
Mutation load, defned as the proportion of deleterious
alleles and genotypes carrying these alleles at the genome-
wide level, has been used as a metric to infer the genetic
health and extinction risk of species or populations that have
experienced severe or consistent demographic bottlenecks
(Robinson et al. 2019; Grossen et al. 2020), maintained
long-term small effective sizes (Robinson et al. 2016), or
been affected by recent anthropogenic activities (Yang et al.
2018; van der Valk et al. 2019). In bottlenecked populations,
genetic drift is likely to eliminate a fraction of deleterious
alleles (Glémin 2003; Mathur and DeWoody 2021; van der
Valk et al. 2021), for these variants are often found at rel-
atively low frequencies at the time of demographic decline
(Mezmouk and Ross-Ibarra 2014; Perrier et al. 2017). By
the same token, however, drift is also capable of increasing
the frequency of another fraction of deleterious alleles
(Romiguier et al. 2014; Renaut and Rieseberg 2015; Ochoa
and Gibbs 2021), leading some of them to the point of fxa-
tion (Benazzo et al. 2017).
Despite recent studies suggesting that sustained drift
could reduce overall proportions of deleterious alleles in
small populations (Mathur and DeWoody 2021; Ochoa and
Gibbs 2021), there remains a concern that persistent delete-
rious alleles in these populations may be redistributed into
a disproportionately high number of homozygous genotypes
given genetic isolation, inbreeding, and ineffcient purifying
selection (Hedrick and Garcia-Dorado 2016). Under such
scenarios, individuals are prone to expressing a mosaic of del-
eterious traits with negative effects on their ftness, collectively
termed inbreeding depression (Frankham 1995; Hedrick
and Kalinowski 2000; Charlesworth and Willis 2009).
Consequently, the proportion of deleterious homozygotes at
the genome-wide level refects minimum realized levels of mu-
tation load (Mathur and DeWoody 2021), as deleterious alleles
present in the heterozygous state could still manifest in the
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