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Genetic consequences of long-term small effective population size in the critically endangered pygmy hog.

ABSTRACT: Increasing human disturbance and climate change have a major impact on habitat integrity and size, with far-reaching consequences for wild fauna and flora. Specifically, population decline and habitat fragmentation result in small, isolated populations. To what extend different endangered species can cope with small population size is still largely unknown. Studies on the genomic landscape of these species can shed light on past demographic dynamics and current genetic load, thereby also providing guidance for conservation programs. The pygmy hog (Porcula salvania) is the smallest and rarest wild pig in the world, with current estimation of only a few hundred living in the wild. Here, we analyzed whole-genome sequencing data of six pygmy hogs, three from the wild and three from a captive population, along with 30 pigs representing six other Suidae. First, we show that the pygmy hog had a very small population size with low genetic diversity over the course of the past ~1 million years. One indication of historical small effective population size is the absence of mitochondrial variation in the six sequenced individuals. Second, we evaluated the impact of historical demography. Runs of homozygosity (ROH) analysis suggests that the pygmy hog population has gone through past but not recent inbreeding. Also, the long-term, extremely small population size may have led to the accumulation of harmful mutations suggesting that the accumulation of deleterious mutations is exceeding purifying selection in this species. Thus, care has to be taken in the conservation program to avoid or minimize the potential for further inbreeding depression, and guard against environmental changes in the future.

SUBMITTER: Liu L

PROVIDER: S-EPMC7980308 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

Project description:Many waterbird populations have become increasingly dependent on agricultural habitats for feeding. While habitat destruction has been proposed as a key reason forcing waterbirds to move from natural habitats to agricultural habitats, few have used long-term data to test this hypothesis. The Siberian crane (Leucogeranus leucogeranus) is an IUCN Critically Endangered species. About 98% of its global population winters at Poyang Lake, China. Recently, many cranes shifted from feeding in natural wetlands to agricultural habitats. Here, we integrate bird surveys, Vallisneria tuber (the traditional food of cranes in natural wetlands) surveys, water level data, and remotely sensed images from 1999 to 2016 to explore the drivers of this habitat shift. Changes in Siberian crane numbers in natural wetlands and agricultural fields indicated that the habitat shift occurred in the winters of 2015-2016. Analyses using generalized linear mixed models suggested that crane numbers in natural wetlands were positively related to tuber density and the interaction between dry season (October-March) water level and tuber density. The changes in tuber density and dry season water level in 2015-2016 indicated that tuber disappearance may have been the primary driver of the habitat shift, with a smaller effect of high water level. Submerged plants at Poyang Lake have degraded seriously in the past two decades. The plant degradation at Shahu Lake, a sublake of Poyang Lake, may have been caused by high spring water, high winter temperature, and low summer temperature. However, the drivers of tuber disappearance at Poyang Lake may not be restricted to these variables. Because Poyang Lake is an important refuge for many waterbirds in the Yangtze River floodplain, it is urgent to take effective measures to restore its submerged plants and ecosystem health. Agricultural fields can be important refuges for Siberian cranes, mitigating the negative impacts of wetland deterioration.

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Genetic consequences of long-term small effective population size in the critically endangered pygmy hog.

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