Genetic effects of long-term captive breeding on the endangered pygmy hog

Long-term captive populations often accumulate genetic changes that are detrimental to their survival in the wild. Periodic genetic evaluation of captive populations is thus necessary to identify deleterious changes and minimize their impact through planned breeding. Pygmy hog (Porcula salvania) is an endangered species with a small population inhabiting the tall sub-Himalayan grasslands of Assam, India. A conservation breeding program of pygmy hog from six founders has produced a multi-generational captive population destined for reintroduction into the wild. However, the impact of conservation breeding on its genetic diversity remained undocumented. Here, we evaluate temporal genetic changes in 39 pygmy hogs from eight consecutive generations of a captive population using genome-wide SNPs, mitochondrial genomes, and MHC sequences, and explore the relationship between genetic diversity and reproductive success. We find that pygmy hog harbors a very low genome-wide heterozygosity (H) compared to other members of the Suidae family. However, within the captive population we find excess heterozygosity and a significant increase in H from the wild-caught founders to the individuals in subsequent generations due to the selective pairing strategy. The MHC and mitochondrial nucleotide diversities were lower in captive generations compared to the founders with a high prevalence of low-frequency MHC haplotypes and more unique mitochondrial genomes. Further, even though no signs of genetic inbreeding were observed from the estimates of individual inbreeding coefficient F and between individuals (FIS) in each generation, the kinship coefficient showed a slightly increasing trend in the recent generations, due to a relatively smaller non-random sample size compared to the entire captive population. Surprisingly, male pygmy hogs that had higher heterozygosity also showed lower breeding success. We briefly discuss the implications of our findings in the context of breeding management and recommend steps to minimize the genetic effects of long-term captive breeding.

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Captive management and the maintenance of genetic diversity in a vulnerable marsupial, the greater bilby

Australian Mammalogy ◽

10.1071/am14009 ◽

2015 ◽

Vol 37 (2) ◽

pp. 170 ◽

Cited By ~ 6

Author(s):

Emily J. Miller ◽

Mark D. B. Eldridge ◽

Keith Morris ◽

Neil Thomas ◽

Catherine A. Herbert

Keyword(s):

Genetic Diversity ◽

Captive Breeding ◽

Natural Habitat ◽

Species Conservation ◽

Molecular Data ◽

Breeding Programs ◽

Captive Populations ◽

Genetic Impact ◽

Captive Breeding Programs

The endemic Australian greater bilby (Macrotis lagotis) is a vulnerable and iconic species. It has declined significantly due to habitat loss, as well as competition and predation from introduced species. Conservation measures include a National Recovery Plan that incorporates several captive breeding programs. Two of these programs were established within 12 months of one another (1997/98), with the same number and sex ratio of founding individuals, but executed different breeding strategies: (1) unmanipulated mating in semi–free range natural habitat versus (2) minimising mean kinship in large enclosures, with the supplementation of new individuals into both populations. This study evaluates the long-term genetic impact of these programs and examines the congruency between the pedigree studbook estimates of diversity and molecular data. Our data demonstrate that genetic diversity was maintained in both populations, with the supplementation of new individuals contributing to the gene pool. The studbook estimates of diversity and inbreeding are not consistent with the microsatellite data and should not solely be relied upon to evaluate the genetic health of captive populations. Our analyses suggest that captive breeding programs may not require costly and intensive management to effectively maintain long-term genetic diversity in a promiscuous species.

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Genome-wide analysis of ivermectin response by Onchocerca volvulus reveals that genetic drift and soft selective sweeps contribute to loss of drug sensitivity

10.1101/094540 ◽

2016 ◽

Cited By ~ 2

Author(s):

Stephen R. Doyle ◽

Catherine Bourguinat ◽

Hugues C. Nana-Djeunga ◽

Jonas A. Kengne-Ouafo ◽

Sébastien D.S. Pion ◽

...

Keyword(s):

Genetic Diversity ◽

Next Generation Sequencing ◽

Genetic Drift ◽

Onchocerca Volvulus ◽

Molecular Pathways ◽

Ivermectin Treatment ◽

Genetic Changes ◽

Genome Wide ◽

Parasite Populations ◽

Generation Sequencing

ABSTRACTBackgroundTreatment of onchocerciasis using mass ivermectin administration has reduced morbidity and transmission throughout Africa and Central/South America. Mass drug administration is likely to exert selection pressure on parasites, and phenotypic and genetic changes in several Onchocerca volvulus populations from Cameroon and Ghana - exposed to more than a decade of regular ivermectin treatment - have raised concern that sub-optimal responses to ivermectin’s anti-fecundity effect are becoming more frequent and may spread.Methodology/Principal FindingsPooled next generation sequencing (Pool-seq) was used to characterise genetic diversity within and between 108 adult female worms differing in ivermectin treatment history and response. Genome-wide analyses revealed genetic variation that significantly differentiated good responder (GR) and sub-optimal responder (SOR) parasites. These variants were not randomly distributed but clustered in ~31 quantitative trait loci (QTLs), with little overlap in putative QTL position and gene content between countries. Published candidate ivermectin SOR genes were largely absent in these regions; QTLs differentiating GR and SOR worms were enriched for genes in molecular pathways associated with neurotransmission, development, and stress responses. Finally, single worm genotyping demonstrated that geographic isolation and genetic change over time (in the presence of drug exposure) had a significantly greater role in shaping genetic diversity than the evolution of SOR.Conclusions/SignificanceThis study is one of the first genome-wide association analyses in a parasitic nematode, and provides insight into the genomics of ivermectin response and population structure of O. volvulus. We argue that ivermectin response is a polygenically-determined quantitative trait in which identical or related molecular pathways but not necessarily individual genes likely determine the extent of ivermectin response in different parasite populations. Furthermore, we propose that genetic drift rather than genetic selection of SOR is the underlying driver of population differentiation, which has significant implications for the emergence and potential spread of SOR within and between these parasite populations.Author summaryOnchocerciasis is a human parasitic disease endemic across large areas of Sub-Saharan Africa, where more that 99% of the estimated 100 million people globally at-risk live. The microfilarial stage of Onchocerca volvulus causes pathologies ranging from mild itching to visual impairment and ultimately, irreversible blindness. Mass administration of ivermectin kills microfilariae and has an anti-fecundity effect on adult worms by temporarily inhibiting the development in utero and/or release into the skin of new microfilariae, thereby reducing morbidity and transmission. Phenotypic and genetic changes in some parasite populations that have undergone multiple ivermectin treatments in Cameroon and Ghana have raised concern that sub-optimal response to ivermectin’s anti-fecundity effect may increase in frequency, reducing the impact of ivermectin-based control measures. We used next generation sequencing of small pools of parasites to define genome-wide genetic differences between phenotypically characterised good and sub-optimal responder parasites from Cameroon and Ghana, and identified multiple genomic regions differentiating the response types. These regions were largely different between parasites from both countries but revealed common molecular pathways that might be involved in determining the extent of response to ivermectin’s anti-fecundity effect. These data reveal a more complex than previously described pattern of genetic diversity among O. volvulus populations that differ in their geography and response to ivermectin treatment.

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Genetic and species-level biodiversity patterns are linked by demography and ecological opportunity

10.1101/2020.06.03.132092 ◽

2020 ◽

Author(s):

Chloé Schmidt ◽

Stéphane Dray ◽

Colin J. Garroway

Keyword(s):

Genetic Diversity ◽

Species Richness ◽

Gene Diversity ◽

Spatial Scales ◽

Ecological Opportunity ◽

Biogeographic Patterns ◽

Genome Wide ◽

Diversity Gradients ◽

Low Levels

AbstractSpecies richness and genetic diversity are the two most fundamental products of evolution. Both are important conservation targets—species richness contributes to ecosystem functioning and human wellbeing, while genetic diversity allows those species to respond to changes in their environment and persist in the long-term. Biogeographic patterns of species richness are well-described, but we know little about patterns of genome-wide genetic diversity at similar spatial scales. Further, despite considerable attention to latitudinal trends in species richness, we still do not have a solid empirical understanding of the various processes that produce them, how they interact, or how they affect genetic diversity. Here we show that genome-wide genetic diversity and species richness share spatial structure, however, species richness hotspots tend to harbor low levels of within-species genetic variation. A single model encompassing eco-evolutionary processes related to environmental energy availability, niche availability, and proximity to humans explained 75% of variation in gene diversity and 90% of the variation in species richness. Our empirical model of both levels of biodiversity supports theory and demonstrates the importance of carrying capacity and ecological opportunity at individual and species levels for generating continent-wide genetic and species diversity gradients.

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Disentangling the mechanisms of mate choice in a captive koala population

10.7287/peerj.preprints.3487v1 ◽

2017 ◽

Author(s):

Parice A Brandies ◽

Catherine E Grueber ◽

Jamie A Ivy ◽

Carolyn J Hogg ◽

Professor K Belov

Keyword(s):

Mate Choice ◽

Female Choice ◽

Mating Success ◽

Captive Breeding ◽

Genetic Determinants ◽

Term Survival ◽

Breeding Programs ◽

Captive Populations ◽

Genome Wide ◽

Captive Breeding Programs

Successful captive breeding programs are crucial to the long-term survival of threatened species. However, pair incompatibility limits sustainability of many captive populations. Understanding whether the drivers of this incompatibility are behavioural or genetic, or a combination of both, is crucial to improving breeding programs. We used twenty-eight years of pairing data from the San Diego Zoo koala colony, plus genetic analyses using both MHC-linked and non-MHC-linked microsatellite markers, to show that both behavioural and genetic determinants can influence mating success. Male age was reconfirmed to be a contributing factor to the likelihood of a pair copulating. Familiarity was also reconfirmed to increase the probability of a successful copulation. Our data provided evidence that females select mates based on MHC and genome-wide similarity. Male heterozygosity at class II MHC loci influenced both pre- and post-copulatory female choice. Genome-wide similarity and similarity at the MHCII DAB locus were also found to influence female choice at the post-copulatory level. Finally, certain MHC-linked alleles were associated with increased or decreased mating success. We predict that utilising a variety of behavioural and MHC-dependent mate choice mechanisms improves female fitness through increased reproductive success. This study highlights the complexity of mate choice mechanisms within a species and the importance of ascertaining mate choice mechanisms to improve the success of captive breeding programs.

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Genomics of sorghum local adaptation to a parasitic plant

10.1101/633529 ◽

2019 ◽

Cited By ~ 1

Author(s):

Emily S. Bellis ◽

Elizabeth A. Kelly ◽

Claire M. Lorts ◽

Huirong Gao ◽

Victoria L. DeLeo ◽

...

Keyword(s):

Genetic Diversity ◽

Local Adaptation ◽

Striga Hermonthica ◽

Wild Plant ◽

Parasitic Weed ◽

Genome Wide ◽

Staple Crop ◽

Term Maintenance ◽

Maintenance Of Diversity

ABSTRACTHost-parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential tradeoffs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and belowground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with tradeoffs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR-Cas9 edited sorghum further indicate the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.SIGNIFICANCE STATEMENTUnderstanding co-evolution in crop-parasite systems is critical to management of myriad pests and pathogens confronting modern agriculture. In contrast to wild plant communities, parasites in agricultural ecosystems are usually expected to gain the upper hand in co-evolutionary ‘arms races’ due to limited genetic diversity of host crops in cultivation. Here, we develop a framework to characterize associations between genome variants in global landraces (traditional varieties) of the staple crop sorghum with the distribution of the devastating parasitic weed Striga hermonthica. We find long-term maintenance of diversity in genes related to parasite resistance, highlighting an important role of host adaptation for co-evolutionary dynamics in smallholder agroecosystems.

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The interplay of population dynamics and the evolutionary process

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1990.0196 ◽

1990 ◽

Vol 330 (1257) ◽

pp. 253-259 ◽

Cited By ~ 8

Keyword(s):

Genetic Diversity ◽

Interspecific Interactions ◽

Genotypic Variation ◽

Evolutionary Process ◽

Interactive System ◽

Population Fluctuations ◽

Genetic Changes ◽

Local Extinctions ◽

Term Maintenance

Long-term maintenance of genetic diversity is affected by ecological forces that are driven in turn by current levels of genetic variation. The strength of population regulation and the consequent patterns of population fluctuations determine the likelihood of genetic changes considered pivotal for rapid speciation. However, genetic diversity in the susceptibility to regulatory forces can reduce the magnitude of such fluctuations and minimize the likelihood of genetic revolutions. A group of populations that experiences local extinctions and recolonizations may hold lower levels of genetic diversity than in the absence of such extinctions, but local adaption, which provides enhanced genetic diversity, can reduce the likelihood of local extinctions. Tightly regulated populations experience different selection pressures than poorly regulated populations, although tighter regulation itself can evolve. When genotypic variation affects the outcome of interspecific interactions on a local scale, this effect, coupled with appropriate spatial variation, can enhance the resilience of the interactive system.

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Genetic stability of Aedes aegypti populations following invasion by wMel Wolbachia

BMC Genomics ◽

10.1186/s12864-021-08200-1 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Meng-Jia Lau ◽

Thomas L. Schmidt ◽

Qiong Yang ◽

Jessica Chung ◽

Lucien Sankey ◽

...

Keyword(s):

Aedes Aegypti ◽

Disease Transmission ◽

Geographic Location ◽

Infection Status ◽

Population Differences ◽

Outlier Analysis ◽

Genetic Changes ◽

Genome Wide ◽

And Behavior

Abstract Background Wolbachia wMel is the most commonly used strain in rear and release strategies for Aedes aegypti mosquitoes that aim to inhibit the transmission of arboviruses such as dengue, Zika, Chikungunya and yellow fever. However, the long-term establishment of wMel in natural Ae. aegypti populations raises concerns that interactions between Wolbachia wMel and Ae. aegypti may lead to changes in the host genome, which could affect useful attributes of Wolbachia that allow it to invade and suppress disease transmission. Results We applied an evolve-and-resequence approach to study genome-wide genetic changes in Ae. aegypti from the Cairns region, Australia, where Wolbachia wMel was first introduced more than 10 years ago. Mosquito samples were collected at three different time points in Gordonvale, Australia, covering the phase before (2010) and after (2013 and 2018) Wolbachia releases. An additional three locations where Wolbachia replacement happened at different times across the last decade were also sampled in 2018. We found that the genomes of mosquito populations mostly remained stable after Wolbachia release, with population differences tending to reflect the geographic location of the populations rather than Wolbachia infection status. However, outlier analysis suggests that Wolbachia may have had an influence on some genes related to immune response, development, recognition and behavior. Conclusions Ae. aegypti populations remained geographically distinct after Wolbachia wMel releases in North Australia despite their Wolbachia infection status. At some specific genomic loci, we found signs of selection associated with Wolbachia, suggesting potential evolutionary impacts can happen in the future and further monitoring is warranted.

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Disentangling the mechanisms of mate choice in a captive koala population

10.7287/peerj.preprints.3487 ◽

2017 ◽

Author(s):

Parice A Brandies ◽

Catherine E Grueber ◽

Jamie A Ivy ◽

Carolyn J Hogg ◽

Professor K Belov

Keyword(s):

Mate Choice ◽

Female Choice ◽

Mating Success ◽

Captive Breeding ◽

Genetic Determinants ◽

Term Survival ◽

Breeding Programs ◽

Captive Populations ◽

Genome Wide ◽

Captive Breeding Programs

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Genetic Status and Management of California Condors

The Condor ◽

10.1093/condor/106.2.215 ◽

2004 ◽

Vol 106 (2) ◽

pp. 215-228 ◽

Cited By ~ 6

Author(s):

Katherine Ralls ◽

Jonathan D. Ballou

Keyword(s):

Genetic Diversity ◽

Captive Breeding ◽

Total Population ◽

Population Bottleneck ◽

Captive Population ◽

Base Population ◽

California Condor ◽

Current Population ◽

Genetic Status ◽

Gymnogyps Californianus

Abstract The last wild California Condor (Gymnogyps californianus) was brought into captivity in 1987. Captive breeding was successful and reintroduction efforts began in 1992. The current population is descended from 14 individuals belonging to three genetic “clans.” This population bottleneck led to the loss of genetic variation and changes in allele frequencies, including a probable increase in the frequency of the putative allele for chondrodystrophy, a lethal form of dwarfism. We use studbook data to analyze the current genetic and demographic status of the population and explain how it is managed to meet specific goals. In August 2002 the population consisted of 206 individuals distributed among three captive-breeding facilities and three reintroduction sites. The population is managed to preserve genetic diversity using the concept of mean kinship. Growth of the total population has been between 10% and 15% per year since 1987, but the growth of the captive population has been only about 5% per year since 1992 due to the removal of chicks for reintroduction. Assuming that founding birds within clans were half-siblings, the birds used to found the captive population theoretically contained 92% of the heterozygosity present in the hypothetical wild base population. About 99.5% of this heterozygosity has been retained in the current population. Alleles from most founders are well represented across captive- breeding facilities and reintroduction sites. The genetic status of this population compares favorably with other species that have been rescued from extinction by captive breeding. Situación Genética y Manejo de Gymnogyps californianus Resumen. El último cóndor californiano (Gymnogyps californianus) silvestre fue puesto en cautiverio en 1987. La reproducción en cautiverio fue exitosa y las reintroducciones comenzaron en 1992. La población actual desciende de 14 individuos pertenecientes a tres “clanes” genéticos. Este cuello de botella poblacional dió lugar a la pérdida de variabilidad genética y a cambios en la frecuencia de alelos, incluyendo un probable incremento en la frecuencia del alelo para condrodistrofia, una forma letal de enanismo. En este estudio, utilizamos datos del libro genealógico para analizar la situación genética y demográfica actual de la población y para explicar cómo se está manejando la población para cumplir con metas específicas. En agosto del 2002 la población consistía de 206 individuos distribuidos en tres instalaciones de reproducción en cautiverio y tres sitios de reintroducción. La población fue manejada con el propósito de conservar la diversidad genética usando el concepto de parentesco medio. El crecimiento de la población ha sido de entre 10% y 15% por año desde 1987, pero el crecimiento de la población en cautiverio ha sido únicamente de aproximadamente un 5% por año desde 1992 debido a la remoción de los pollos para su reintroducción. Suponiendo que los cóndores fundadores dentro de cada clan eran medio- hermanos, las aves que fueron utilizadas para fundar la población en cautiverio teóricamente contienen un 92% de la heterocigosidad presente en la población silvestre base hipotética. Cerca de un 99.5% de esta heterocigosidad ha sido retenida en la población actual. Alelos de la mayoría de los fundadores están bien representados en las diversas instalaciones de reproducción en cautiverio y sitios de reintroducción. La situación de esta población parece ser mejor que la de otras especies silvestres que han sido rescatadas por medio de la reproducción en cautiverio.

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Genetic risks of supplementing trout populations with native stocks: a simulation case study from current Pyrenean populations

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/cjfas-2013-0362 ◽

2014 ◽

Vol 71 (8) ◽

pp. 1243-1255 ◽

Cited By ~ 10

Author(s):

Raquel Fernández-Cebrián ◽

Rosa Maria Araguas ◽

Nuria Sanz ◽

Jose Luis García-Marín

Keyword(s):

Salmo Trutta ◽

Captive Breeding ◽

Gene Diversity ◽

Genetic Changes ◽

Study Region ◽

Local Diversity ◽

Genetic Risks ◽

Complex Population ◽

Brown Trout Salmo Trutta

The risks of supplementation must be examined to assess the genetic effects to native wild populations before full implementation or exclusion of programs that involve captive breeding and release. Real genetic data can be applied to simulations of genetic changes in populations of interest and subsequently used in risk assessment. Ancestral Mediterranean brown trout (Salmo trutta) lineages exhibit complex population structure among native populations. Genetically divergent Atlantic stocks were maintained and released in the Mediterranean rivers as recreational fish, which resulted in hybridization and introgression with local populations. Therefore, we designed a new supplementation program based on native stocks and evaluated the genetic risks associated with releasing native fish in recreational fisheries. Our simulation was delimited by the observed population genetic structure and available hatchery facilities in the study region. Supplementation with native stocks maintained estimates of gene diversity indexes (total diversity (HT), local diversity (HS), and population differentiation (GST)). However, simulations indicated that long-term supplementation significantly reduced genetic diversity among locations because of a homogenizing effect of populations along each management unit. Therefore, such reinforcements compromised the conservation of local genetic variation. Nevertheless, replacement of current foreign stocks with native stocks can be an important step towards promoting the value of preserving local diversity among anglers.

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