The far-reaching effects of genetic process in a keystone predator species, grey wolves.

Although detrimental genetic processes are known to adversely affect the viability of populations, little is known about how detrimental genetic processes in a keystone species can affect the functioning of ecosystems. Here, we assessed how changes in the genetic characteristics of a keystone predator, grey wolves, affected the ecosystem of Isle Royale National Park over two decades. Changes in the genetic characteristic of the wolf population associated with a genetic rescue event, followed by high levels of inbreeding, led to a rise and then fall in predation rates on moose, the primary prey of wolves and dominant mammalian herbivore in this system. Those changes in predation rate led to large fluctuations in moose abundance, which in turn affected browse rates on balsam fir, the dominant forage for moose during winter and an important boreal forest species. Thus, forest dynamics can be traced back to changes in the genetic characteristics of a predator population.

The crucial role of genome-wide genetic variation in conservation.

The unprecedented rate of extinction calls for efficient use of genetics to help conserve biodiversity. Several recent genomic and simulation-based studies have argued that the field of conservation biology has placed too much focus on conserving genome-wide genetic variation, and that the field should instead focus on managing the subset of functional genetic variation that is thought to affect fitness. Here, we critically evaluate the feasibility and likely benefits of this approach in conservation. We find that population genetics theory and empirical results show that conserving genome-wide genetic variation is generally the best approach to prevent inbreeding depression and loss of adaptive potential from driving populations toward extinction. Focusing conservation efforts on presumably functional genetic variation will only be feasible occasionally, often misleading, and counterproductive when prioritized over genome-wide genetic variation. Given the increasing rate of habitat loss and other environmental changes, failure to recognize the detrimental effects of lost genome-wide genetic variation on long-term population viability will only worsen the biodiversity crisis.

Comment on "Individual heterozygosity predicts translocation success in threatened desert tortoises".

Scott et al (Reports, 27 November 2020, p. 1086) suggest, on the basis of conclusions obtained from a desert tortoise reintroduction program, that higher genomic heterozygosity should be used to identify individuals for successful translocation. I contend that this recommendation is questionable given these relocated tortoises' unknown origin, their high mortality, insufficient data on resident tortoises and other components of fitness, and potential allelic dropout.

Galapagos Islands Endemic Vertebrates: A Population Genetics Perspective.

The organisms of the Galapagos Islands played a central role in the development of the theory of evolution by Charles Darwin. Examination of the population genetics factors of many of these organisms with modern molecular methods has expanded our understanding of their evolution. Here, I provide a perspective on how selection, gene flow, genetic drift, mutation, and inbreeding have contributed to the evolution of 6 iconic Galapagos species: flightless cormorant, pink iguana, marine iguana, Galapagos hawk, giant tortoises, and Darwin's finches. Because of the inherent biological differences among these species that have colonized the Galapagos, different population genetic factors appear to be more or less important in these different species. For example, the Galapagos provided novel environments in which strong selection took place and the Darwin's finches diversified to produce new species and the cormorant adapted to the nutrient-rich western shores of the Galapagos by losing its ability to fly and genomic data have now identified candidate genes. In both the pink iguana, which exists in one small population, and the Galapagos hawk, which has small population sizes, genetic drift has been potentially quite important. There appears to be very limited interisland gene flow in the flightless cormorant and the Galapagos hawk. On the other hand, both the marine iguana and some of the Darwin's finches appear to have significant interisland gene flow. Hybridization between species and subspecies has also introduced new adaptive variation, and in some cases, hybridization might have resulted in despeciation. Overall, new population genetics and genomics research has provided additional insight into the evolution of vertebrate species in the Galapagos.

Negative-Assortative Mating in the White-Throated Sparrow.

Nonrandom mating based on phenotype has been observed in a number of organisms, but a very high proportion of these examples are of assortative mating. The strongest example of negative-assortative mating is for white-striped versus tan-striped crown in the white-throated sparrow, where about 98% of the observed pairings (mated pairs or social pairs) are between mates with different phenotypes and the correlation between mating types is -0.964. Although nonrandom mating has been explored theoretically for decades, these models have generally not focused on specific well-documented examples. Here we have developed a model to investigate the dynamics and equilibrium of this iconic example. The observed pattern of mating appears to be the result of 96% negative-assortative mating and a 17% advantage of W (white) male × T (tan) female matings compared to the reciprocal T male × W female matings. The equilibrium heterozygosity given these values is 0.500, very close to the 0.501 observed in our large sample of pairings, and this heterozygosity has been maintained for the 29 years from 1988 to 2016. In addition, the equilibrium frequency of 2m inversion determining the white-striped phenotype has been maintained at a frequency very close to its equilibrium frequency of 0.25. Overall, this model demonstrates how evolutionary genetic models can be used to understand negative-assortative mating.

Ancestry dynamics in a South American population: The impact of gene flow and preferential mating.

OBJECTIVES: European ancestry in many populations in Latin America at autosomal loci is often higher than that from X-linked loci indicating more European male ancestry and more Amerindian female ancestry. Generally, this has been attributed to more European male gene flow but could also result from an advantage to European mating or reproductive success. METHODS: Population genetic models were developed to investigate the dynamics of gene flow and mating or reproductive success. Using estimates of autosomal and X-chromosome European ancestry, the amount of male gene flow or mating or reproductive advantage for Europeans, or those with European ancestry, was estimated. RESULTS: In a population from Antioquia, Colombia with an estimated 79% European autosomal ancestry and an estimated 69% European X-chromosome ancestry, about 15% male gene flow from Europe or about 20% mating or reproductive advantage of Europeans over Amerindians resulted in these levels of European ancestry in the contemporary population. Combinations of gene flow and mating advantage were nearly additive in their impact. CONCLUSIONS: Gene flow, mating advantage, or a combination of both factors, are consistent with observed levels of European ancestry in a Latin American population. This approach provides a general methodology to determine the levels of gene flow and mating differences that can explain the observed contemporary differences in ancestry from autosomes and X-chromosomes.

Assortative Mating and Linkage Disequilibrium.

Assortative mating has been suggested to result in an increase in heritability and additive genetic variance through an increase in linkage disequilibrium. The impact of assortative mating on linkage disequilibrium was explicitly examined for the two-locus model of Wright (1921) and two selective assortative mating models. For the Wright (1921) model, when the proportion of assortative mating was high, positive linkage disequilibrium was generated. However, when the proportion of assortative mating was similar to that found in some studies, the amount of linkage disequilibrium was quite low. In addition, the amount of linkage disequilibrium was independent of the level of recombination. For two selective assortative models, the amount of linkage disequilibrium was a function of the amount of recombination. For these models, the linkage disequilibrium generated was negative mainly because repulsion heterozygotes were favored over coupling heterozygotes. From these findings, the impact of assortative mating on linkage disequilibrium, and consequently heritability and additive genetic variance, appears to be small and model-specific.

Genomic Variation of Inbreeding and Ancestry in the Remaining Two Isle Royale Wolves.

Inbreeding, relatedness, and ancestry have traditionally been estimated with pedigree information, however, molecular genomic data can provide more detailed examination of these properties. For example, pedigree information provides estimation of the expected value of these measures but molecular genomic data can estimate the realized values of these measures in individuals. Here, we generate the theoretical distribution of inbreeding, relatedness, and ancestry for the individuals in the pedigree of the Isle Royale wolves, the first examination of such variation in a wild population with a known pedigree. We use the 38 autosomes of the dog genome and their estimated map lengths in our genomic analysis. Although it is known that the remaining wolves are highly inbred, closely related, and descend from only 3 ancestors, our analyses suggest that there is significant variation in the realized inbreeding and relatedness around pedigree expectations. For example, the expected inbreeding in a hypothetical offspring from the 2 remaining wolves is 0.438 but the realized 95% genomic confidence interval is from 0.311 to 0.565. For individual chromosomes, a substantial proportion of the whole chromosomes are completely identical by descent. This examination provides a background to use when analyzing molecular genomic data for individual levels of inbreeding, relatedness, and ancestry. The level of variation in these measures is a function of the time to the common ancestor(s), the number of chromosomes, and the rate of recombination. In the Isle Royale wolf population, the few generations to a common ancestor results in the high variance in genomic inbreeding.

Understanding Inbreeding Depression, Purging, and Genetic Rescue.

Inbreeding depression, the reduction of fitness caused by inbreeding, is a nearly universal phenomenon that depends on past mutation, selection, and genetic drift. Recent estimates suggest that its impact on individual fitness is even greater than previously thought. Genomic information is contributing to its detection and can enlighten important aspects of its genetic architecture. In natural populations, purging and genetic rescue mitigate fitness decline during inbreeding periods, and might be critical to population survival, thus, both mechanisms should be considered when assessing extinction risks. However, deliberate purging and genetic rescue involve considerable risk in the short and medium term, so that neither appears to be a panacea against high inbreeding depression.

Negative-assortative mating for color in wolves.

There is strong negative-assortative mating for gray and black pelage color in the iconic wolves in Yellowstone National Park. This is the first documented case of significant negative-assortative mating in mammals and one of only a very few cases in vertebrates. Of 261 matings documented from 1995 to 2015, 63.6% were between gray and black wolves and the correlation between mates for color was -0.266. There was a similar excess of matings of both gray males × black females and black males × gray females. Using the observed frequency of negative-assortative mating in a model with both random and negative-assortative mating, the estimated proportion of negative-assortative mating was 0.430. The estimated frequency of black wolves in the population from 1996 to 2014 was 0.452 and these frequencies appear stable over this 19-year period. Using the estimated level of negative-assortative mating, the predicted equilibrium frequency of the dominant allele was 0.278, very close to the mean value of 0.253 observed. In addition, the patterns of genotype frequencies, that is, the observed proportion of black homozygotes and the observed excess of black heterozygotes, are consistent with negative-assortative mating. Importantly these results demonstrate that negative-assortative mating could be entirely responsible for the maintenance of this well-known color polymorphism.

Examining the cause of high inbreeding depression: analysis of whole-genome sequence data in 28 selfed progeny of Eucalyptus grandis.

The genome-wide heterozygosity at 9590 genes, all heterozygous in a single Eucalyptus grandis parent tree, was examined in a group of 28 S1 offspring. Heterozygosity ranged from 52-79%, averaging 65.5%, much higher than the 50% expected under random segregation, supporting the occurrence of strong (47%) selection against homozygosity. The expected pattern of heterozygosity from theoretical calculations and simulations for recessive detrimentals (pseudo-overdominance) and intrinsic heterozygote advantage was examined and compared with that observed. The observed patterns are consistent with at least several detrimental loci with large effects on both parental chromosomes of the 11 pairs. It is likely that 100 or more genes, many with substantial effects on viability, are contributing to this inbreeding depression. Although our genome-wide analysis of nearly 10 000 genes strongly suggested that pseudo-overdominance was responsible for the observed high inbreeding depression, heterozygote advantage could not be excluded. Finding inconvertible evidence of the cause of inbreeding depression still presents a difficult challenge. This study is the first theoretical examination of the genomic effect of inbreeding in a forest tree and provides an approach to analyze these data to determine the extent and cause of inbreeding depression across other plant genomes.

Estimation of Male Gene Flow: Use Caution.

Because male gene flow cannot easily be estimated directly in many organisms, Hedrick et al. (2013) provided an approach to estimate male gene flow given estimates of diploid nuclear and female differentiation. This approach appears to work well when there is lower female than male gene flow. However, in a tiger data set there was less female differentiation observed as estimated by mitochondrial DNA than expected given the observed overall nuclear diploid differentiation. To analyze these data, we suggest an alternative approach which allows incorporation of sex-specific gene flow and sex-specific effective population size. We find that the pattern of differentiation observed in tigers was consistent with a lower male than female effective population size using this alternative approach. Further, this finding is consistent with observed data in tigers where the male effective population size was 33% that of the female effective population size.