scholarly journals Detecting inbreeding depression in a severely bottlenecked, recovering species: The little spotted kiwi (Apteryx owenii)

2021 ◽  
Author(s):  
◽  
Helen R. Taylor
Keyword(s):  
Genetic Variation ◽  
Population Growth ◽  
Inbreeding Depression ◽  
Hatching Success ◽  
Extinction Risk ◽  
Long Island ◽  
Island Population ◽  
Valuable Insight ◽  
Inbreeding Coefficients

<p>Population bottlenecks reduce genetic variation and population size. Small populations are at greater risk of inbreeding, which further erodes genetic diversity and can lead to inbreeding depression. Inbreeding depression is known to increase extinction risk. Thus, detecting inbreeding depression is important for population viability assessment and conservation management. However, identifying inbreeding depression in wild populations is challenging due to the difficulty of obtaining long-term measures of fitness and error-free measures of individual inbreeding coefficients. I investigated inbreeding depression and our power to detect it in species that have very low genetic variation, using little spotted kiwi (Apteryx owenii) (LSK) as a case study. This endemic New Zealand ratite experienced a bottleneck of, at most, five individuals ~100 years ago and has since been subjected to secondary bottlenecks as a result of introductions to new predator-free locations. There is no behavioural pedigree data available for any LSK population and the status of the species is monitored almost exclusively via population growth. I conducted two seasons of field work to determine hatching success in the two LSK populations with the highest and lowest numbers of founders; Zealandia Sanctuary (40 founders) and Long Island (two founders). I also used simulation-based modelling to assess the feasibility of reconstructing pedigrees based on individual genotypes from LSK populations to calculate pedigree inbreeding coefficients. Finally, I used microsatellite genotypes to measure the genetic erosion in successive filial groupings of Long Island and Zealandia LSK as a result of their respective bottlenecks, and tested for inbreeding depression on Long Island. Hatching success was significantly lower on Long Island than in Zealandia in both years of the study despite significantly higher reproductive effort on Long Island. Although this was suggestive of inbreeding depression on Long Island, simulation results showed that constructing a pedigree for any LSK population based on the genetic markers and samples currently available would lead to inaccurate pedigrees and invalid estimates of individual inbreeding coefficients. Thus, an alternative method of detecting inbreeding and inbreeding depression was required. Microsatellite data showed continued loss of heterozygosity in both populations, but loss of allelic diversity on Long Island only. Individual genotypes indicated that the majority (74%) of the adult Long Island population is comprised of the founding pair (F) and their direct offspring (F1) rather than birds from subsequent generations (F2+). This is not what would be expected if survival was equal between these two filial classes. I suggest that the high levels of inbreeding (≥0.25) in F2+ birds is impacting on their survival, creating a demographic skew in the population and resulting in lower hatching success on average on Long Island when compared to the relatively outbred Zealandia birds. This inbreeding depression appears to have been masked, thus far, by positive population growth on Long Island resulting from the long life span of LSK (27-83 years) and continued reproductive success of the founding pair. Thus, it is likely that the Long Island population will go into decline when the founding pair cease to reproduce. This study highlights the challenges of measuring inbreeding depression in species with very low genetic variation and the importance of assessing the statistical power and reliability of the genetic tools available for those species. It also demonstrates that basic genetic techniques can offer valuable insight when more advanced tools prove error-prone. Monitoring vital rates such as hatching success in conjunction with genetic data is important for assessing the success of conservation translocations and detecting potentially cryptic genetic threats such as inbreeding depression. My results suggest that LSK are being affected by inbreeding depression and that careful genetic management will be required to ensure the long-term viability of this species.</p>

scholarly journals Detecting inbreeding depression in a severely bottlenecked, recovering species: The little spotted kiwi (Apteryx owenii)

2021 ◽  
Author(s):  
◽  
Helen R. Taylor
Keyword(s):  
Genetic Variation ◽  
Population Growth ◽  
Inbreeding Depression ◽  
Hatching Success ◽  
Extinction Risk ◽  
Long Island ◽  
Island Population ◽  
Valuable Insight ◽  
Inbreeding Coefficients

<p>Population bottlenecks reduce genetic variation and population size. Small populations are at greater risk of inbreeding, which further erodes genetic diversity and can lead to inbreeding depression. Inbreeding depression is known to increase extinction risk. Thus, detecting inbreeding depression is important for population viability assessment and conservation management. However, identifying inbreeding depression in wild populations is challenging due to the difficulty of obtaining long-term measures of fitness and error-free measures of individual inbreeding coefficients. I investigated inbreeding depression and our power to detect it in species that have very low genetic variation, using little spotted kiwi (Apteryx owenii) (LSK) as a case study. This endemic New Zealand ratite experienced a bottleneck of, at most, five individuals ~100 years ago and has since been subjected to secondary bottlenecks as a result of introductions to new predator-free locations. There is no behavioural pedigree data available for any LSK population and the status of the species is monitored almost exclusively via population growth. I conducted two seasons of field work to determine hatching success in the two LSK populations with the highest and lowest numbers of founders; Zealandia Sanctuary (40 founders) and Long Island (two founders). I also used simulation-based modelling to assess the feasibility of reconstructing pedigrees based on individual genotypes from LSK populations to calculate pedigree inbreeding coefficients. Finally, I used microsatellite genotypes to measure the genetic erosion in successive filial groupings of Long Island and Zealandia LSK as a result of their respective bottlenecks, and tested for inbreeding depression on Long Island. Hatching success was significantly lower on Long Island than in Zealandia in both years of the study despite significantly higher reproductive effort on Long Island. Although this was suggestive of inbreeding depression on Long Island, simulation results showed that constructing a pedigree for any LSK population based on the genetic markers and samples currently available would lead to inaccurate pedigrees and invalid estimates of individual inbreeding coefficients. Thus, an alternative method of detecting inbreeding and inbreeding depression was required. Microsatellite data showed continued loss of heterozygosity in both populations, but loss of allelic diversity on Long Island only. Individual genotypes indicated that the majority (74%) of the adult Long Island population is comprised of the founding pair (F) and their direct offspring (F1) rather than birds from subsequent generations (F2+). This is not what would be expected if survival was equal between these two filial classes. I suggest that the high levels of inbreeding (≥0.25) in F2+ birds is impacting on their survival, creating a demographic skew in the population and resulting in lower hatching success on average on Long Island when compared to the relatively outbred Zealandia birds. This inbreeding depression appears to have been masked, thus far, by positive population growth on Long Island resulting from the long life span of LSK (27-83 years) and continued reproductive success of the founding pair. Thus, it is likely that the Long Island population will go into decline when the founding pair cease to reproduce. This study highlights the challenges of measuring inbreeding depression in species with very low genetic variation and the importance of assessing the statistical power and reliability of the genetic tools available for those species. It also demonstrates that basic genetic techniques can offer valuable insight when more advanced tools prove error-prone. Monitoring vital rates such as hatching success in conjunction with genetic data is important for assessing the success of conservation translocations and detecting potentially cryptic genetic threats such as inbreeding depression. My results suggest that LSK are being affected by inbreeding depression and that careful genetic management will be required to ensure the long-term viability of this species.</p>

Heterozygosity-Fitness Correlations in a Continental Island Population of Thorn-Tailed Rayadito

2020 ◽  
Author(s):  
Esteban Botero-Delgadillo ◽  
Verónica Quirici ◽  
Rodrigo A Vásquez ◽  
Bart Kempenaers
Keyword(s):  
Inbreeding Depression ◽  
Nonlinear Effects ◽  
Molecular Techniques ◽  
Laying Date ◽  
Island Population ◽  
Apparent Survival ◽  
Linear Effect ◽  
Fledging Success ◽  
Gradual Process

Abstract Heterozygosity-fitness correlations (HFCs) have been used to monitor the effects of inbreeding in threatened populations. HFCs can also be useful to investigate the potential effects of inbreeding in isolated relict populations of long-term persistence and to better understand the role of inbreeding and outbreeding as drivers of changes in genetic diversity. We studied a continental island population of thorn-tailed rayadito (Aphrastura spinicauda) inhabiting the relict forest of Fray Jorge National Park, north-central Chile. This population has experienced a long-term, gradual process of isolation since the end of the Tertiary. Using 10 years of field data in combination with molecular techniques, we tested for HFCs to assess the importance of inbreeding depression. If inbreeding depression is important, we predict a positive relationship between individual heterozygosity and fitness-related traits. We genotyped 183 individuals at 12 polymorphic microsatellite loci and used 7 measures of reproductive success and estimates of apparent survival to calculate HFCs. We found weak to moderate statistical support (P-values between 0.05 and 0.01) for a linear effect of female multi-locus heterozygosity (MLH) on clutch size and nonlinear effects on laying date and fledging success. While more heterozygous females laid smaller clutches, nonlinear effects indicated that females with intermediate values of MLH started laying earlier and had higher fledging success. We found no evidence for effects of MLH on annual fecundity or on apparent survival. Our results along with the long-term demographic stability of the study population contradict the hypothesis that inbreeding depression occurs in this population.

scholarly journals Genetic consequences of a century of protection: serial founder events and survival of the little spotted kiwi ( Apteryx owenii )

2013 ◽  
Vol 280 (1762) ◽  
pp. 20130576 ◽  
Author(s):  
Kristina M. Ramstad ◽  
Rogan M. Colbourne ◽  
Hugh A. Robertson ◽  
Fred W. Allendorf ◽  
Charles H. Daugherty
Keyword(s):  
Genetic Variation ◽  
Long Island ◽  
Genetic Bottleneck ◽  
Island Population ◽  
Mating Pair ◽  
Terrestrial Vertebrates ◽  
Census Size ◽  
Single Mating ◽  
Genetic Bottlenecks ◽  
Founder Events

We present the outcome of a century of post-bottleneck isolation of a long-lived species, the little spotted kiwi ( Apteryx owenii , LSK) and demonstrate that profound genetic consequences can result from protecting few individuals in isolation. LSK were saved from extinction by translocation of five birds from South Island, New Zealand to Kapiti Island 100 years ago. The Kapiti population now numbers some 1200 birds and provides founders for new populations. We used 15 microsatellite loci to compare genetic variation among Kapiti LSK and the populations of Red Mercury, Tiritiri Matangi and Long Islands that were founded with birds from Kapiti. Two LSK native to D'Urville Island were also placed on Long Island. We found extremely low genetic variation and signatures of acute and recent genetic bottleneck effects in all four populations, indicating that LSK have survived multiple genetic bottlenecks. The Long Island population appears to have arisen from a single mating pair from Kapiti, suggesting there is no genetic contribution from D'Urville birds among extant LSK. The N e / N C ratio of Kapiti Island LSK (0.03) is exceptionally low for terrestrial vertebrates and suggests that genetic diversity might still be eroding in this population, despite its large census size.

Inbreeding and Inbreeding Depression

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.

Unprecedented Low Levels of Genetic Variation and Inbreeding Depression in an Island Population of the Black-Footed Rock-Wallaby

1999 ◽  
Vol 13 (3) ◽  
pp. 531-541 ◽  
Author(s):  
Mark D. B. Eldridge ◽  
Juliet M. King ◽  
Anne K. Loupis ◽  
Peter B. S. Spencer ◽  
Andrea C. Taylor ◽  
...  
Keyword(s):  
Genetic Variation ◽  
Inbreeding Depression ◽  
Island Population ◽  
Low Levels

Long term effects of outbreeding: experimental founding of island population eliminates malformations and improves hatching success in sand lizards

2020 ◽  
Vol 249 ◽  
pp. 108710
Author(s):  
Willow R. Lindsay ◽  
Thomas Madsen ◽  
Erik Wapstra ◽  
Mette Lillie ◽  
Lisa Loeb ◽  
...  
Keyword(s):  
Hatching Success ◽  
Island Population ◽  
Long Term Effects

scholarly journals Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation

2020 ◽  
pp. 201909599
Author(s):  
Alina K. Niskanen ◽  
Anna M. Billing ◽  
Håkon Holand ◽  
Ingerid J. Hagen ◽  
Yimen G. Araya-Ajoy ◽  
...  
Keyword(s):  
Inbreeding Depression ◽  
House Sparrow ◽  
Extinction Risk ◽  
Demographic History ◽  
Natural Populations ◽  
Ecological Factors ◽  
Genomic Tools ◽  
Subdivided Populations ◽  
Modern Genomic

Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations.

scholarly journals Sensitive males: inbreeding depression in an endangered bird

2010 ◽  
Vol 277 (1700) ◽  
pp. 3677-3684 ◽  
Author(s):  
Patricia Brekke ◽  
Peter M. Bennett ◽  
Jinliang Wang ◽  
Nathalie Pettorelli ◽  
John G. Ewen
Keyword(s):  
Inbreeding Depression ◽  
Threatened Species ◽  
Genetic Load ◽  
Early Life History ◽  
Molecular Sexing ◽  
Life History Stages ◽  
Inbreeding Coefficients ◽  
Nestling Development ◽  
Autosomal Microsatellite Loci

Attempts to conserve threatened species by establishing new populations via reintroduction are controversial. Theory predicts that genetic bottlenecks result in increased mating between relatives and inbreeding depression. However, few studies of wild sourced reintroductions have carefully examined these genetic consequences. Our study assesses inbreeding and inbreeding depression in a free-living reintroduced population of an endangered New Zealand bird, the hihi ( Notiomystis cincta ). Using molecular sexing and marker-based inbreeding coefficients estimated from 19 autosomal microsatellite loci, we show that (i) inbreeding depresses offspring survival, (ii) male embryos are more inbred on average than female embryos, (iii) the effect of inbreeding depression is male-biased and (iv) this population has a substantial genetic load. Male susceptibility to inbreeding during embryo and nestling development may be due to size dimorphism, resulting in faster growth rates and more stressful development for male embryos and nestlings compared with females. This work highlights the effects of inbreeding at early life-history stages and the repercussions for the long-term population viability of threatened species.

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

2021 ◽  
Author(s):  
Noelia Perez-Pereira ◽  
Armando Caballero ◽  
Aurora Garcia-Dorado
Keyword(s):  
Inbreeding Depression ◽  
Extinction Risk ◽  
Conservation Strategy ◽  
Recessive Mutation ◽  
Stable Gene ◽  
Main Concern ◽  
Genetic Rescue ◽  
Genetic Purging ◽  
The Impact

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.

scholarly journals Predicting evolutionary rescue via evolving plasticity in stochastic environments

2016 ◽  
Vol 283 (1839) ◽  
pp. 20161690 ◽  
Author(s):  
Jaime Ashander ◽  
Luis-Miguel Chevin ◽  
Marissa L. Baskett
Keyword(s):  
Genetic Variation ◽  
Phenotypic Plasticity ◽  
Extinction Risk ◽  
Environmental Stochasticity ◽  
High Plasticity ◽  
Cryptic Genetic Variation ◽  
Stochastic Environments ◽  
Evolutionary Rescue ◽  
Stochastic Demography

Phenotypic plasticity and its evolution may help evolutionary rescue in a novel and stressful environment, especially if environmental novelty reveals cryptic genetic variation that enables the evolution of increased plasticity. However, the environmental stochasticity ubiquitous in natural systems may alter these predictions, because high plasticity may amplify phenotype–environment mismatches. Although previous studies have highlighted this potential detrimental effect of plasticity in stochastic environments, they have not investigated how it affects extinction risk in the context of evolutionary rescue and with evolving plasticity. We investigate this question here by integrating stochastic demography with quantitative genetic theory in a model with simultaneous change in the mean and predictability (temporal autocorrelation) of the environment. We develop an approximate prediction of long-term persistence under the new pattern of environmental fluctuations, and compare it with numerical simulations for short- and long-term extinction risk. We find that reduced predictability increases extinction risk and reduces persistence because it increases stochastic load during rescue. This understanding of how stochastic demography, phenotypic plasticity, and evolution interact when evolution acts on cryptic genetic variation revealed in a novel environment can inform expectations for invasions, extinctions, or the emergence of chemical resistance in pests.

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