Temporal changes in allele frequency, genetic variation and inbreeding depression in small populations of the guppy, Poecilia reticulata

Conservation biology as a discipline focused on endangered species is young and dates only from the late 1970s. Although conservation of endangered species encompasses many different biological disciplines, including behavior, ecology, and genetics, evolutionary considerations always have been emphasized (e.g., Frankel and Soule 1981). Many of the applications of evolutionary concepts to conservation are ones related to genetic variation in small or subdivided populations. However, the critical status of many endangered species makes both more precision and more caution necessary than the general findings for evolutionary considerations. On the other hand, the dire situations of many endangered species often require recommendations to be made on less than adequate data. Overall, one can think of the evolutionary aspects of conservation biology as an applied aspect of the evolution of small populations with the important constraint that any conclusions or recommendations may influence the actual extinction of the populations or species under consideration. From this perspective, all of the factors that influence continuing evolution (i.e., selection, inbreeding, genetic drift, gene flow, and mutation; e.g., Hedrick 2000) are potentially important in conservation. The evolutionary issues of widest concern in conservation biology—inbreeding depression and maintenance of genetic variation— can be seen in their simplest form as the joint effects of inbreeding and selection, and of genetic drift and mutation, respectively. However, even in model organisms such as Drosophila, the basis of inbreeding depression and the maintenance of genetic variation are not clearly understood. In addition, findings from model laboratory organisms may not provide good insight into problems in many endangered species, the most visible of which are generally slowly reproducing, large vertebrates with small populations. Here we will first focus on introductions to two important evolutionary aspects of conservation biology: the units of conservation and inbreeding depression. Then, we will discuss studies in two organisms as illustrations of these and related principles—an endangered fish species, the Gila topminnow, and desert bighorn sheep—to illustrate some evolutionary aspects of conservation. In the discussion, we will mention some of the other evolutionary topics that are relevant to conservation biology.

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Three types of rescue can avert extinction in a changing environment

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1504732112 ◽

2015 ◽

Vol 112 (33) ◽

pp. 10557-10562 ◽

Cited By ~ 73

Author(s):

Ruth A. Hufbauer ◽

Marianna Szűcs ◽

Emily Kasyon ◽

Courtney Youngberg ◽

Michael J. Koontz ◽

...

Keyword(s):

Genetic Variation ◽

Genetic Variability ◽

Inbreeding Depression ◽

Small Populations ◽

Genetic Rescue ◽

Microcosm Experiment ◽

High Quality ◽

Evolutionary Rescue ◽

Population Sizes ◽

Number Of Individuals

Setting aside high-quality large areas of habitat to protect threatened populations is becoming increasingly difficult as humans fragment and degrade the environment. Biologists and managers therefore must determine the best way to shepherd small populations through the dual challenges of reductions in both the number of individuals and genetic variability. By bringing in additional individuals, threatened populations can be increased in size (demographic rescue) or provided with variation to facilitate adaptation and reduce inbreeding (genetic rescue). The relative strengths of demographic and genetic rescue for reducing extinction and increasing growth of threatened populations are untested, and which type of rescue is effective may vary with population size. Using the flour beetle (Tribolium castaneum) in a microcosm experiment, we disentangled the genetic and demographic components of rescue, and compared them with adaptation from standing genetic variation (evolutionary rescue in the strictest sense) using 244 experimental populations founded at either a smaller (50 individuals) or larger (150 individuals) size. Both types of rescue reduced extinction, and those effects were additive. Over the course of six generations, genetic rescue increased population sizes and intrinsic fitness substantially. Both large and small populations showed evidence of being able to adapt from standing genetic variation. Our results support the practice of genetic rescue in facilitating adaptation and reducing inbreeding depression, and suggest that demographic rescue alone may suffice in larger populations even if only moderately inbred individuals are available for addition.

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Inbreeding reduces reproductive fitness

10.1093/oso/9780198783398.003.0003 ◽

2017 ◽

Author(s):

Richard Frankham ◽

Jonathan D. Ballou ◽

Katherine Ralls ◽

Mark D. B. Eldridge ◽

Michele R. Dudash ◽

...

Keyword(s):

Natural Selection ◽

Inbreeding Depression ◽

Reproductive Fitness ◽

Heterozygote Advantage ◽

Small Populations ◽

Population Bottlenecks ◽

Risk Of Extinction ◽

Survival And Reproduction

The harmful impacts of inbreeding are generally greater in species that naturally outbreed compared to those in inbreeding species, greater in stressful than benign environments, greater for fitness than peripheral traits, and greater for total fitness compared to its individual components. Inbreeding reduces survival and reproduction (i.e., it causes inbreeding depression), and thereby increases the risk of extinction. Inbreeding depression is due to increased homozygosity for harmful alleles and at loci exhibiting heterozygote advantage. Natural selection may remove (purge) the alleles that cause inbreeding depression, especially following inbreeding or population bottlenecks, but it has limited effects in small populations and usually does not completely eliminate inbreeding depression. Inbreeding depression is nearly universal in sexually reproducing organisms that are diploid or have higher ploidies.

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Testing temporal changes in allele frequencies: a simulation approach

Genetics Research ◽

10.1017/s0016672310000339 ◽

2010 ◽

Vol 92 (4) ◽

pp. 309-320 ◽

Cited By ~ 14

Author(s):

EDSON SANDOVAL-CASTELLANOS

Keyword(s):

Molecular Data ◽

Temporal Changes ◽

Allele Frequencies ◽

Small Populations ◽

Simulation Approach ◽

Simulation Test ◽

Agent Based ◽

Binomial Sampling ◽

Molecular Databases ◽

Parameter Values

SummaryAnalysis of the temporal variation in allele frequencies is useful for studying microevolutionary processes. However, many statistical methods routinely used to test temporal changes in allele frequencies fail to establish a proper hypothesis or have theoretical or practical limitations. Here, a Bayesian statistical test is proposed in which the distribution of the distances among sampling frequencies is approached with computer simulations, and hypergeometric sampling is considered instead of binomial sampling. To validate the test and compare its performance with other tests, agent-based model simulations were run for a variety of scenarios, and two real molecular databases were analysed. The results showed that the simulation test (ST) maintained the significance value used (α=0·05) for a vast combination of parameter values, whereas other tests were sensitive to the effect of genetic drift or binomial sampling. The differences between binomial and hypergeometric sampling were more complex than expected, and a novel effect was described. This study suggests that the ST is especially useful for studies with small populations and many alleles, as in microsatellite or sequencing molecular data.

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Geographic patterns of human allele frequency variation: a variant-centric perspective

10.1101/2020.07.01.182311 ◽

2020 ◽

Author(s):

Arjun Biddanda ◽

Daniel P. Rice ◽

John Novembre

Keyword(s):

Genetic Variation ◽

Gene Flow ◽

Genetic Structure ◽

Allele Frequency ◽

Human Genetics ◽

Geographic Region ◽

Frequency Variation ◽

Human Genetic Variation ◽

Alternative Representation ◽

Geographic Patterns

AbstractA key challenge in human genetics is to describe and understand the distribution of human genetic variation. Often genetic variation is described by showing relationships among populations or individuals, in each case drawing inferences over a large number of variants. Here, we present an alternative representation of human genetic variation that reveals the relative abundance of different allele frequency patterns across populations. This approach allows viewers to easily see several features of human genetic structure: (1) most variants are rare and geographically localized, (2) variants that are common in a single geographic region are more likely to be shared across the globe than to be private to that region, and (3) where two individuals differ, it is most often due to variants that are common globally, regardless of whether the individuals are from the same region or different regions. To guide interpretation of the results, we also apply the visualization to contrasting theoretical scenarios with varying levels of divergence and gene flow. Our variant-centric visualization clarifies the major geographic patterns of human variation and can be used to help correct potential misconceptions about the extent and nature of genetic differentiation among populations.

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Severe Habitat Fragmentation Leads to Declines in Genetic Variation, Mate Availability, and Reproductive Success in Small Populations of a Once-Common Australian Grassland Daisy

International Journal of Plant Sciences ◽

10.1086/673242 ◽

2013 ◽

Vol 174 (9) ◽

pp. 1209-1218 ◽

Cited By ~ 10

Author(s):

John W. Morgan ◽

Michaela J. Meyer ◽

Andrew G. Young

Keyword(s):

Genetic Variation ◽

Habitat Fragmentation ◽

Reproductive Success ◽

Small Populations ◽

Mate Availability

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Unique Genomic and Phenotypic Responses to Extreme and Variable pH Conditions in Purple Urchin Larvae

Integrative and Comparative Biology ◽

10.1093/icb/icaa072 ◽

2020 ◽

Vol 60 (2) ◽

pp. 318-331

Author(s):

April D Garrett ◽

Reid S Brennan ◽

Anya L Steinhart ◽

Aubrey M Pelletier ◽

Melissa H Pespeni

Keyword(s):

Genetic Variation ◽

Allele Frequency ◽

Sea Urchin ◽

Genetic Basis ◽

Adaptive Genetic Variation ◽

Protein Coding ◽

Purple Sea Urchin ◽

Ph Conditions ◽

Frequency Changes ◽

Genetic Responses

Synopsis Environmental variation experienced by a species across space and time can promote the maintenance of genetic diversity that may be adaptive in future global change conditions. Selection experiments have shown that purple sea urchin, Strongylocentrotus purpuratus, populations have adaptive genetic variation for surviving pH conditions at the “edge” (pH 7.5) of conditions experienced in nature. However, little is known about whether populations have genetic variation for surviving low-pH events beyond those currently experienced in nature or how variation in pH conditions affects organismal and genetic responses. Here, we quantified survival, growth, and allele frequency shifts in experimentally selected developing purple sea urchin larvae in static and variable conditions at three pH levels: pH 8.1 (control), pH 7.5 (edge-of-range), and pH 7.0 (extreme). Variable treatments recovered body size relative to static treatments, but resulted in higher mortality, suggesting a potential tradeoff between survival and growth under pH stress. However, within each pH level, allele frequency changes were overlapping between static and variable conditions, suggesting a shared genetic basis underlying survival to mean pH regardless of variability. In contrast, genetic responses to pH 7.5 (edge) versus pH 7.0 (extreme) conditions were distinct, indicating a unique genetic basis of survival. In addition, loci under selection were more likely to be in exonic regions than regulatory, indicating that selection targeted protein-coding variation. Loci under selection in variable pH 7.5 conditions, more similar to conditions periodically experienced in nature, performed functions related to lipid biosynthesis and metabolism, while loci under selection in static pH 7.0 conditions performed functions related to transmembrane and mitochondrial processes. While these results are promising in that purple sea urchin populations possess genetic variation for surviving extreme pH conditions not currently experienced in nature, they caution that increased acidification does not result in a linear response but elicits unique physiological stresses and survival mechanisms.

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Population size, habitat fragmentation, and the nature of adaptive variation in a stream fish

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2014.0370 ◽

2014 ◽

Vol 281 (1790) ◽

pp. 20140370 ◽

Cited By ~ 31

Author(s):

Dylan J. Fraser ◽

Paul V. Debes ◽

Louis Bernatchez ◽

Jeffrey A. Hutchings

Keyword(s):

Genetic Variation ◽

Habitat Fragmentation ◽

Population Size ◽

Brook Trout ◽

Small Populations ◽

Adaptive Genetic Variation ◽

Genetic Population ◽

Fragmented Populations ◽

Large Populations ◽

Adaptive Differentiation

Whether and how habitat fragmentation and population size jointly affect adaptive genetic variation and adaptive population differentiation are largely unexplored. Owing to pronounced genetic drift, small, fragmented populations are thought to exhibit reduced adaptive genetic variation relative to large populations. Yet fragmentation is known to increase variability within and among habitats as population size decreases. Such variability might instead favour the maintenance of adaptive polymorphisms and/or generate more variability in adaptive differentiation at smaller population size. We investigated these alternative hypotheses by analysing coding-gene, single-nucleotide polymorphisms associated with different biological functions in fragmented brook trout populations of variable sizes. Putative adaptive differentiation was greater between small and large populations or among small populations than among large populations. These trends were stronger for genetic population size measures than demographic ones and were present despite pronounced drift in small populations. Our results suggest that fragmentation affects natural selection and that the changes elicited in the adaptive genetic composition and differentiation of fragmented populations vary with population size. By generating more variable evolutionary responses, the alteration of selective pressures during habitat fragmentation may affect future population persistence independently of, and perhaps long before, the effects of demographic and genetic stochasticity are manifest.

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Inbreeding and Inbreeding Depression

Evolutionary Biology ◽

10.1093/obo/9780199941728-0124 ◽

2020 ◽

Author(s):

Donald M. Waller ◽

Lukas F. Keller

Keyword(s):

Genetic Variation ◽

Inbreeding Depression ◽

Charles Darwin ◽

Extinction Risk ◽

Random Mating ◽

Genetic Material ◽

Great Length ◽

Genetic Rescue ◽

Isolated Populations ◽

Genetic Transmission

Inbreeding (also referred to as “consanguinity”) occurs when mates are related to each other due to incest, assortative mating, small population size, or population sub-structuring. Inbreeding results in an excess of homozygotes and hence a deficiency of heterozygotes. This, in turn, exposes recessive genetic variation otherwise hidden by heterozygosity with dominant alleles relative to random mating. Interest in inbreeding arose from its use in animal and plant breeding programs to expose such variation and to fix variants in genetically homogenous lines. Starting with Gregor Mendel’s experiments with peas, geneticists have widely exploited inbreeding as a research tool, leading R. C. Lewontin to conclude that “Every discovery in classical and population genetics has depended on some sort of inbreeding experiment” (see Lewontin’s 1965 article “The Theory of Inbreeding.” Science 150:1800–1801). Charles Darwin wrote an entire book on the effects of inbreeding as measured in fifty-two taxa of plants. He and others noted that most plants and animals go to great length to avoid inbreeding, suggesting that inbreeding has high costs that often outweigh the benefits of inbreeding. Benefits of inbreeding include increased genetic transmission while the costs of inbreeding manifest as inbreeding depression when deleterious, mostly recessive alleles otherwise hidden as heterozygotes emerge in homozygote form upon inbreeding. Inbreeding also reduces fitness when heterozygotes are more fit than both homozygotes, but such overdominance is rare. Recurrent mutation continuously generates deleterious recessive alleles that create a genetic “load” of deleterious mutations mostly hidden within heterozygotes in outcrossing populations. Upon inbreeding, the load is expressed when deleterious alleles segregate as homozygotes, causing often substantial inbreeding depression. Although inbreeding alone does not change allele frequencies, it does redistribute genetic variation, reducing it within families or populations while increasing it among families or populations. Inbreeding also increases selection by exposing deleterious recessive mutations, a process called purging that can deplete genetic variation. For all these reasons, inbreeding is a central concept in evolutionary biology. Inbreeding is also central to conservation biology as small and isolated populations become prone to inbreeding and thus suffer inbreeding depression. Inbreeding can reduce population viability and increase extinction risk by reducing individual survival and/or reproduction. Such effects can often be reversed, however, by introducing new genetic material that re-establishes heterozygosity (“genetic rescue”). The current availability of DNA sequence and expression data is now allowing more detailed analyses of the causes and evolutionary consequences of inbreeding.

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