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Polygenic plague resistance in the great gerbil uncovered by population sequencing.

ABSTRACT: Pathogens can elicit high selective pressure on hosts, potentially altering genetic diversity over short evolutionary timescales. Intraspecific variation in immune response is observable as variable survivability from specific infections. The great gerbil (Rhombomys opimus) is a rodent plague host with a heterogenic but highly resistant phenotype. Here, we investigate the genomic basis for plague-resistant phenotypes by exposing wild-caught great gerbils to plague (Yersinia pestis). Whole genome sequencing of 10 survivors and 10 moribund individuals revealed a subset of genomic regions showing elevated differentiation. Gene ontology analysis of candidate genes in these regions demonstrated enrichment of genes directly involved in immune functions, cellular metabolism and the regulation of apoptosis as well as pathways involved in transcription, translation, and gene regulation. Transcriptomic analysis revealed that the early activated great gerbil immune response to plague consisted of classical components of the innate immune system. Our approach combining challenge experiments with transcriptomics and population level sequencing, provides new insight into the genetic background of plague-resistance and confirms its complex nature, most likely involving multiple genes and pathways of both the immune system and regulation of basic cellular functions.

SUBMITTER: Nilsson P

PROVIDER: S-EPMC9802093 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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Polygenic plague resistance in the great gerbil uncovered by population sequencing.

Nilsson Pernille P Ravinet Mark M Cui Yujun Y Berg Paul R PR Zhang Yujiang Y Guo Rong R Luo Tao T Song Yajun Y Trucchi Emiliano E Hoff Siv N K SNK Lv Ruichen R Schmid Boris V BV Easterday W Ryan WR Jakobsen Kjetill S KS Stenseth Nils Chr NC Yang Ruifu R Jentoft Sissel S

PNAS nexus 20221005 5

Pathogens can elicit high selective pressure on hosts, potentially altering genetic diversity over short evolutionary timescales. Intraspecific variation in immune response is observable as variable survivability from specific infections. The great gerbil (<i>Rhombomys opimus</i>) is a rodent plague host with a heterogenic but highly resistant phenotype. Here, we investigate the genomic basis for plague-resistant phenotypes by exposing wild-caught great gerbils to plague (<i>Yersinia pestis</i>) ...[more]

PMID: 36712379

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Project description:BackgroundThe great gerbil (Rhombomys opimus), whose ectoparasitic fleas significantly influence the transmission and prevalence of plague, was the dominant rodent species in the Junggar Basin in Northwestern China. However, the distribution pattern of fleas parasitizing the great gerbils and whether that pattern affected the intensity of plague prevalence in different regions remains unclear.MethodsA total of 17,780 fleas were collected from 2258 great gerbils throughout 90 investigations. This study focused on analyzing the rate of flea infestation and the flea indices of species that parasitized the great gerbils. The aggregation patterns of fleas parasitizing the great gerbils were measured using the parameter b of Taylor's power law, and the differences in the aggregation index of plague epidemic areas were compared.ResultsWe observed an aggregated distribution of ectoparasitic fleas in the great gerbils. The aggregation degree of combined fleas was higher (P > 0.05) in the eastern area of the Junggar Basin than in the western area. The primary species of ectoparasitic fleas of the great gerbils were Xenopsylla skrjabini, Xenopsylla minax, Xenopsylla hirtipes, and Nosopsyllus laeviceps laiveceps. X. skrjabini exhibited the highest (P < 0.01) degree of aggregation in the eastern zone (III), with an aggregation index of 1.61. In addition, in the middle zone (II), the aggregation index of X. minax and X. hirtipes reached their peak, with values of 1.53 and 1.56, respectively. Conversely, the degree of aggregation of N. laeviceps was more pronounced in the eastern zone than in the western zone of the Junggar Basin. Notably, the aggregation degree of the combined fleas of the great gerbils during the low-intensity plague epidemic period, with an index of 1.93, was significantly higher (P < 0.001) than during the high-intensity epidemic period, with an index of 1.50.ConclusionsFleas exhibited an aggregated distribution within the great gerbil population. The levels of flea aggregation varied across zones characterized by differing intensities of plague epidemics. In addition, the degree of flea aggregation was significantly correlated with the intensity of plague prevalence.

Project description:BackgroundRodents play an important role in the life cycle of ixodid and argasid ticks, particularly as hosts of larvae and nymphs. The great gerbil (Rhombomys opimus), the preferred prey item of several carnivores (e.g. the red fox and marbled polecat), is the dominant rodent species in the Gurbantunggut Desert in northwestern China. The aim of this study was to investigate tick species associated with different hosts in the habitat of great gerbils, including wildlife and livestock.MethodsDuring 2018-2023, ticks were removed from 326 great gerbils, two red foxes (Vulpes vulpes), three marbled polecats (Vormela peregusna), 35 pastured sheep (Ovis aries), and one long-eared desert hedgehog (Hemiechinus auritus) in the Gurbantunggut Desert. Ticks were identified according to standard morphological keys. Then, they were further analyzed by molecular and phylogenic methods based on two mitochondrial markers, 16S rDNA and cytochrome c oxidase subunit I (COI) genes.ResultsA total of 889 ticks were collected, representing five species. These included Hyalomma asiaticum (n = 425: 24 larvae, 79 nymphs and 322 adults), Rhipicephalus turanicus (n = 153: 2 nymphs and 151 adults), Haemaphysalis erinacei (n = 298: 4 larvae, 7 nymphs and 287 adults), Ixodes acuminatus (n = 7: 4 nymphs and 3 adults) and Ornithodoros tartakovskyi (6 adults). Based on COI sequences, molecular and phylogenetic analyses showed that (i) I. acuminatus from great gerbils and marbled polecats clustered with I. acuminatus reported from Europe; (ii) O. tartakovskyi found in northwestern China belonged to an independent clade; (iii) Hy. asiaticum, R. turanicus and Ha. erinacei had 100% sequence identities to conspecific ticks sampled previously in China.ConclusionsThe great gerbil is an important host for the developmental stages of I. acuminatus, O. tartakovskyi, Ha. erinacei, Hy. asiaticum and R. turanicus, thus supporting the life cycle of several tick species which, as adults, parasitize predators (red fox and marble polecat) as well as pastured sheep and hedgehogs in the Gurbantunggut Desert. Ixodes acuminatus and O. tartakovskyi were found for the first time on great gerbil and marbled polecat, respectively.

Project description:BackgroundOne of the major challenges in evolutionary biology is identifying rare species and devising management plans to protect them while also sustaining their genetic diversity. However, in attempting a broad understanding of rarity, single-species studies provide limited insights because they do not reveal whether the factors that affect rare species differ from those that affect more common species. To illustrate this important concept and to arrive at a better understanding of the form of rarity characterizing the rare Gerbillus henleyi, we explored its population genetic structure alongside that of the locally common Gerbillus andersoni allenbyi. We trapped gerbils in several locations in Israel's western and inner Negev sand dunes. We then extracted DNA from ear samples, and amplified two mitochondrial sequences: the control region (CR) and the cytochrome oxidase 2 gene (CO2).ResultsNucleotide diversity was low for all sequences, especially for the CR of G. a. allenbyi, which showed no diversity. We could not detect any significant population genetic structure in G. henleyi. In contrast, G. a. allenbyi's CO2 sequence showed significant population genetic structure. Pairwise PhiPT comparisons showed low values for G. henleyi but high values for G. a. allenbyi. Analysis of the species' demographic history indicated that G. henleyi's population size has not changed recently, and is under the influence of an ongoing bottleneck. The same analysis for G. a. allenbyi showed that this species has undergone a recent population expansion.ConclusionsComparing the two species, the populations of G. a. allenbyi are more isolated from each other, likely due to the high habitat specificity characterizing this species. The bottleneck pattern found in G. henleyi may be the result of competition with larger gerbil species. This result, together with the broad habitat use and high turnover rate characterizing G. henleyi, may explain the low level of differentiation among its populations. The evidence for a recent population expansion of G. a. allenbyi fits well with known geomorphological data about the formation of the Negev sand dunes and paleontological data about this species' expansion throughout the Levant. In conclusion, we suggest that adopting a comparative approach as presented here can markedly improve our understanding of the causes and effects of rarity, which in turn can allow us to better protect biodiversity patterns.

Dataset Information

Polygenic plague resistance in the great gerbil uncovered by population sequencing.

Publications

Polygenic plague resistance in the great gerbil uncovered by population sequencing.

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