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Research Article | Open Access

Population genomic data reveal low genetic diversity, divergence and local adaptation among threatened Reeves’s Pheasant (Syrmaticus reevesii)

Qi LuaPengcheng WangbJiang ChangcDe ChenaShenghan GaodJacob Höglunde( )Zhengwang Zhanga( )
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, 100875, China
Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Nanjing, 210023, China
State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing, 100012, China
State Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China
Department of Ecology and Genetics, Animal Ecology, Uppsala University, Uppsala, Sweden
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Abstract

Population genomic data could provide valuable information for conservation efforts; however, limited studies have been conducted to investigate the genetic status of threatened pheasants. Reeves’s Pheasant (Syrmaticus reevesii) is facing population decline, attributed to increases in habitat loss. There is a knowledge gap in understanding the genomic status and genetic basis underlying the local adaptation of this threatened bird. Here, we used population genomic data to assess population structure, genetic diversity, inbreeding patterns, and genetic divergence. Furthermore, we identified candidate genes linked with adaptation across the current distribution of Reeves’s Pheasant. The present study assembled the first de novo genome sequence of Reeves’s Pheasant and annotated 19,458 genes. We also sequenced 30 individuals from three populations (Dabie Mountain, Shennongjia, Qinling Mountain) and found that there was clear population structure among those populations. By comparing with other threatened species, we found that Reeves’s Pheasants have low genetic diversity. Runs of homozygosity suggest that the Shennongjia population has experienced serious inbreeding. The demographic history results indicated that three populations experienced several declines during the glacial period. Local adaptative analysis among the populations identified 241 candidate genes under directional selection. They are involved in a large variety of processes, including the immune response and pigmentation. Our results suggest that the three populations should be considered as three different conservation units. The current study provides genetic evidence for conserving the threatened Reeves’s Pheasant and provides genomic resources for global biodiversity management.

References

 
Allendorf, F.W., Luikart, G., 2007. Conserving Global Biodiversity? Conservation and the Genetics of Populations. Blackwell Publishing, Oxford.
 

Alvarado, A.H., Bossu, C.M., Harrigan, R.J., Bay, R.A., Nelson, A.R.P., Smith, T.B., et al., 2022. Genotype-environment associations across spatial scales reveal the importance of putative adaptive genetic variation in divergence. Evol. Appl. 15, 1390–1407.

 
Andrews, S., 2010. FastQC: a quality control tool for high throughput sequence data. In: Babraham Bioinformatics. Babraham Institute, Cambridge.
 

Ashrafzadeh, M.R., Khosravi, R., Fernandes, C., Aguayo, C., Bagi, Z., Lavadinovic, V.M., et al., 2021. Assessing the origin, genetic structure and demographic history of the common pheasant (Phasianus colchicus) in the introduced European range. Sci. Rep. 11, 21721.

 

Bao, Z., Eddy, S.R., 2002. Automated de novo identification of repeat sequence families in sequenced genomes. Genome Res. 12, 1269–1276.

 

Bao, W., Kojima, K.K., Kohany, O., 2015. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mobile DNA 6, 11.

 

Barnosky, A.D., Matzke, N., Tomiya, S., Wogan, G.O., Swartz, B., Quental, T.B., et al., 2011. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57.

 

Bei, Y., Chen, W., Sun, B., Li, J., Lai, J., Meng, S., 2014. Population structure of the endangered Hume’s pheasant (Syrmaticus humiae) inferred from a partial sequence of the mitochondrial DNA control region. Biochem. Syst. Ecol. 57, 69–77.

 

Benson, G., 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580.

 
Bick, J.T., Zeng, S., Robinson, M.D., Ulbrich, S.E., Bauersachs, S., 2019. Mammalian Annotation Database for improved annotation and functional classification of Omics datasets from less well-annotated organisms. Database 2019, doi: 10.1093/database/baz086.
 
BirdLife International, 2018. Syrmaticus reevesii. The IUCN Red List of Threatened Species 2018: e.T22679346A131873938. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22679346A131873938.en. (Accessed 22 December 2023).
 

Bolger, A.M., Lohse, M., Usadel, B., 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.

 

Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., et al., 2009. BLAST+: architecture and applications. BMC Bioinf. 10, 421.

 

Cano, R.J., Poinar, H.N., Pieniazek, N.J., Acra, A., Poinar Jr, G.O., 1993. Amplification and sequencing of DNA from a 120-135-million-year-old weevil. Nature 363, 536–538.

 

Ceballos, F.C., Joshi, P.K., Clark, D.W., Ramsay, M., Wilson, J.F., 2018. Runs of homozygosity: windows into population history and trait architecture. Nat. Rev. Genet. 19, 220–234.

 

Ceballos, G., Ehrlich, P.R., Raven, P.H., 2020. Vertebrates on the brink as indicators of biological annihilation and the sixth mass extinction. P. Natl. Acad. Sci. USA 117, 201922686.

 
Ciofi, C., Funk, S.M., Coote, T., Cheesman, D.J., Hammond, R.L., Saccheri, I.J., et al., 1998. Genotyping with microsatellite markers. In: Karp, A., Isaac, P.G., Ingram, D.S. (Eds.), Molecular Tools for Screening Biodiversity. Springer, Dordrecht, pp. 195–201.
 

CITES, 2019. Convention on International Trade in Endangered Species of Wild Fauna and Flora. CoP18 Prop 18.

 

Danecek, P., Auton, A., Abecasis, G., Albers, C.A., Banks, E., DePristo, M.A., et al., 2011. The variant call format and VCFtools. Bioinformatics 27, 2156–2158.

 

Davis, M.B., Shaw, R.G., 2001. Range shifts and adaptive responses to Quaternary climate change. Science 292, 673–679.

 

Eldridge, M.D.B., Deakin, J.E., MacDonald, A.J., Byrne, M., Fitzgerald, A., Johnson, R.N., et al., 2020. The Oz Mammals Genomics (OMG) initiative: developing genomic resources for mammal conservation at a continental scale. Aust. Zool. 40, 505–509.

 

Ellegren, H., Galtier, N., 2016. Determinants of genetic diversity. Nat. Rev. Genet. 17, 422–433.

 

Falush, D., Stephens, M., Pritchard, J.K., 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.

 

Faria, D.A., Mamani, E.M., Pappas, M.R., Pappas Jr, G.J., Grattapaglia, D., 2010. A selected set of EST-derived microsatellites, polymorphic and transferable across 6 species of Eucalyptus. J. Hered. 101, 512–520.

 

Flynn, J.M., Hubley, R., Goubert, C., Rosen, J., Clark, A.G., Feschotte, C., et al., 2020. RepeatModeler2 for automated genomic discovery of transposable element families. P. Natl. Acad. Sci. USA 117, 9451–9457.

 

Frankham, R., 2005. Genetics and extinction. Biol. Conserv. 126, 131–140.

 

Frankham, R., 2010. Where are we in conservation genetics and where do we need to go? Conserv. Genet. 11, 661–663.

 

Frankham, R., Ballou, J.D., Briscoe, D.A., 2004. A Primer of Conservation Genetics. Cambridge University Press, Cambridge.

 

Garcia, M.B., 2003. Demographic viability of a relict population of the critically endangered plant Borderea chouardii. Conserv. Biol. 17, 1672–1680.

 

Garcia-Alcalde, F., Okonechnikov, K., Carbonell, J., Cruz, L.M., Gotz, S., Tarazona, S., et al., 2012. Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 28, 2678–2679.

 

Gloux, A., Duclos, M.J., Brionne, A., Bourin, M., Nys, Y., Rehault-Godbert, S., 2019. Integrative analysis of transcriptomic data related to the liver of laying hens: from physiological basics to newly identified functions. BMC Genomics 20, 821.

 

Hedrick, P.W., Kalinowski, S.T., 2000. Inbreeding depression in conservation biology. Ann. Rev. Ecol. Syst. 31, 139–162.

 

Hewitt, G.M., 2004. Genetic consequences of climatic oscillations in the Quaternary. Philos. T. Roy. Soc. B 359, 183–195.

 
Höglund, J., 2009. Evolutionary Conservation Genetics. Oxford Academic, Oxford.
 

Hohenlohe, P.A., Funk, W.C., Rajora, O.P., 2021. Population genomics for wildlife conservation and management. Mol. Ecol. 30, 62–82.

 

Holt, C., Yandell, M., 2011. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinf. 12, 491.

 

Hu, Y., Thapa, A., Wei, F., 2020. Ailurus fulgens (Himalayan red panda) and Ailurus styani (Chinese red panda). Trends Genet. 36, 624–625.

 

International Chicken Genome Sequencing Consortium, 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432, 695–716.

 

Jiang, P.P., Lang, Q.L., Fang, S.G., Ding, P., Chen, L.M., 2005. A genetic diversity comparison between captive individuals and wild individuals of Elliot’s Pheasant (Syrmaticus ellioti) using mitochondrial DNA. J. Zhejiang Univ. - Sci. B 6, 413–417.

 

Jurka, J., Kapitonov, V.V., Pavlicek, A., Klonowski, P., Kohany, O., Walichiewicz, J., 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462–467.

 

Kardos, M., Armstrong, E.E., Fitzpatrick, S.W., Hauser, S., Hedrick, P.W., Miller, J.M., et al., 2021. The crucial role of genome-wide genetic variation in conservation. P. Natl. Acad. Sci. USA 118, e2104642118.

 

Kawakami, T., Backstrom, N., Burri, R., Husby, A., Olason, P., Rice, A.M., et al., 2014. Estimation of linkage disequilibrium and interspecific gene flow in F icedula flycatchers by a newly developed 50k single-nucleotide polymorphism array. Mol. Ecol. Resour. 14, 1248–1260.

 

Keane, A., Brooke, M.L., McGowan, P.J.K., 2005. Correlates of extinction risk and hunting pressure in gamebirds (Galliformes). Biol. Conserv. 126, 216–233.

 

Kimura, M., 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge.

 

Kliver, S., Houck, M.L., Perelman, P.L., Totikov, A., Tomarovsky, A., Dudchenko, O., et al., 2023. Chromosome-length genome assembly and karyotype of the endangered black-footed ferret (Mustela nigripes). J. Hered. 114, 539–548.

 

Korf, I., 2004. Gene finding in novel genomes. BMC Bioinf. 5, 59.

 

Korneliussen, T.S., Albrechtsen, A., Nielsen, R., 2014. ANGSD: analysis of next generation sequencing data. BMC Bioinf. 15, 356.

 

Kozma, R., Rodin-Morch, P., Hoglund, J., 2019. Genomic regions of speciation and adaptation among three species of grouse. Sci. Rep. 9, 812.

 

Lande, R., Shannon, S., 1996. The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50, 434–437.

 

Le Luyer, J., Monaco, C.J., Milhade, L., Reisser, C., Soyez, C., Raapoto, H., et al., 2022. Gene expression plasticity, genetic variation and fatty acid remodelling in divergent populations of a tropical bivalve species. J. Anim. Ecol. 91, 1196–1208.

 

Lee, T.H., Guo, H., Wang, X., Kim, C., Paterson, A.H., 2014. SNPhylo: a pipeline to construct a phylogenetic tree from huge SNP data. BMC Genomics 15, 162.

 

Li, H., Durbin, R., 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760.

 

Li, L., Abbott, R.J., Liu, B., Sun, Y., Li, L., Zou, J., et al., 2013. Pliocene intraspecific divergence and Plio-Pleistocene range expansions within Picea likiangensis (Lijiang spruce), a dominant forest tree of the Qinghai-Tibet Plateau. Mol. Ecol. 22, 5237–5255.

 

Li, L., Dong, M., Wang, X-G., 2016. The implication and significance of beta 2 microglobulin: a conservative multifunctional regulator. Chinese Med. J. 129, 448–455.

 

Li, H., Durbin, R., 2011. Inference of human population history from individual whole-genome sequences. Nature 475 (7357), 493–496.

 

Li, X., Liu, T., Li, A., Xiao, Y., Sun, K., Feng, J., 2023. Diversifying selection and climatic effects on major histocompatibility complex class Ⅱ gene diversity in the greater horseshoe bat. Evol. Appl. 16, 688–704.

 

Liu, Y., Liu, S., Zhang, N., Chen, D., Que, P., Liu, N., et al., 2019. Genome assembly of the Common Pheasant Phasianus colchicus: A model for speciation and ecological genomics. Genome Biol. Evol. 11, 3326–3331.

 

Lu, S., Hou, X., Tian, S., Liu, Z., Wang, Y., Jin, T., et al., 2023. Dispersal patterns of Reeves’s pheasant based on genetic and behavioral evidence. Curr. Zool. doi: 10.1093/cz/zoad026.

 
MacKinnon, J., Meng, S., Cheung, C., Carey, G., Zhu, X., Melville, D., 1996. A biodiversity review of China. WWF International China Programme, Hong Kong.
 

Manichaikul, A., Mychaleckyj, J.C., Rich, S.S., Daly, K., Sale, M., Chen, W.M., 2010. Robust relationship inference in genome-wide association studies. Bioinformatics 26, 2867–2873.

 

Mattila, A.L., Duplouy, A., Kirjokangas, M., Lehtonen, R., Rastas, P., Hanski, I., 2012. High genetic load in an old isolated butterfly population. P. Natl. Acad. Sci. USA 109, E2496-E2505.

 

McGowan, P.J.K., Owens, L.L., Grainger, M.J., 2012. Galliformes science and species extinctions: what we know and what we need to know. Anim. Biodivers. Conserv. 35, 321–331.

 

Meyer-Lucht, Y., Mulder, K.P., James, M.C., McMahon, B.J., Buckley, K., Piertney, S.B., et al., 2016. Adaptive and neutral genetic differentiation among Scottish and endangered Irish red grouse (Lagopus lagopus scotica). Conserv. Genet. 17, 615–630.

 

Parra, G., Bradnam, K., Korf, I., 2007. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061–1067.

 

Peixoto, F.P., Braga, P.H.P., Mendes, P., 2018. A synthesis of ecological and evolutionary determinants of bat diversity across spatial scales. BMC Ecol. 18, 18.

 

Perez-Portela, R., Wangensteen, O.S., Garcia-Cisneros, A., Valero-Jimenez, C., Palacin, C., Turon, X., 2019. Spatio-temporal patterns of genetic variation in Arbacia lixula, a thermophilous sea urchin in expansion in the Mediterranean. Heredity 122, 244–259.

 

Poelstra, J.W., Ellegren, H., Wolf, J.B.W., 2013. An extensive candidate gene approach to speciation: diversity, divergence and linkage disequilibrium in candidate pigmentation genes across the European crow hybrid zone. Heredity 111, 467–473.

 

Price, A.L., Jones, N.C., Pevzner, P.A., 2005. De novo identification of repeat families in large genomes. Bioinformatics 21, i351-i358.

 

Privé, F., Luu, K., Vilhjálmsson, B.J., Blum, M.G.B., 2020. Performing highly efficient genome scans for local adaptation with R package pcadapt Version 4. Mol. Biol. Evol. 37, 2153–2154.

 

Rasmussen, P.C., 2004. Threatened Birds of Asia: The BirdLife International Red Data Book. Auk 121, 619–622.

 

Reed, D.H., Frankham, R., 2003. Correlation between fitness and genetic diversity. Conserv. Biol. 17, 230–237.

 

Ren, G., Mateo, R.G., Liu, J., Suchan, T., Alvarez, N., Guisan, A., et al., 2017. Genetic consequences of Quaternary climatic oscillations in the Himalayas: Primula tibetica as a case study based on restriction site-associated DNA sequencing. New Phytol. 213, 1500–1512.

 

Roach, M.J., Johnson, D.L., Bohlmann, J., van Vuuren, H.J.J., Jones, S.J.M., Pretorius, I.S., et al., 2018. Population sequencing reveals clonal diversity and ancestral inbreeding in the grapevine cultivar Chardonnay. PLoS Genet. 14, e1007807.

 

Saremi, N.F., Supple, M.A., Byrne, A., Cahill, J.A., Coutinho, L.L., Dalen, L., et al., 2019. Puma genomes from North and South America provide insights into the genomic consequences of inbreeding. Nat. Commun. 10, 4769.

 

Schou, M.F., Loeschcke, V., Bechsgaard, J., Schlötterer, C., Kristensen, T.N., 2017. Unexpected high genetic diversity in small populations suggests maintenance by associative overdominance. Mol. Ecol. 26, 6510–6523.

 

Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V., Zdobnov, E.M., 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212.

 

Slatkin, M., 2008. Linkage disequilibrium-understanding the evolutionary past and mapping the medical future. Nat. Rev. Genet. 9, 477–485.

 

Spielman, D., Brook, B.W., Briscoe, D.A., Frankham, R., 2004. Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv. Genet. 5, 439–448.

 

Stanke, M., Steinkamp, R., Waack, S., Morgenstern, B., 2004. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 32, W309–W312.

 

Tian, S., Xu, J., Wang, Y., 2020. Human infrastructure development drives decline in suitable habitat for Reeves’s pheasant in the Dabie Mountains in the last 20 years. Global Ecol. Conserv. 22, e00940.

 

Tian, S., Xu, J., Li, J., Zhang, M., Wang, Y., 2021. Response of Reeves’s Pheasants distribution to human infrastructure in the Dabie Mountains over the last 20 years. Animals 11, 2037.

 

Tian, S., Lu, S., Hua, J., Chang, J., Li, J., Zhang, Z., et al., 2022. Integrating habitat suitability modelling and assessment of the conservation gaps of nature reserves for the threatened Reeves’s Pheasant. Bird Conserv. Int. 32, 384–397.

 

Van der Auwera, G.A., Carneiro, M.O., Hartl, C., Poplin, R., Del Angel, G., Levy-Moonshine, A., et al., 2013. From FastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline. Curr. Protoc. Bioinformatics 43, 11.10.1-11.10.33.

 

Vrijenhoek, R.C., 1994. Unisexual fish: model systems for studying ecology and evolution. Ann. Rev. Ecol. Syst. 25, 71–96.

 

Wang, N., Liu, Y., Zhang, Z., 2009. Characterization of nine microsatellite loci for a globally vulnerable species, Reeves’s Pheasant (Syrmaticus reevesii). Conserv. Genet. 10, 1511–1514.

 

Wang, P., Burley, J.T., Liu, Y., Chang, J., Chen, D., Lu, Q., et al., 2021. Genomic consequences of long-term population decline in Brown Eared Pheasant. Mol. Biol. Evol. 38, 263–273.

 

Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.

 

Weisenfeld, N.I., Kumar, V., Shah, P., Church, D.M., Jaffe, D.B., 2017. Direct determination of diploid genome sequences. Genome Res. 27, 757–767.

 

Whitlock, M.C., 2000. Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution 54, 1855–1861.

 

Wickham, H., 2011. ggplot2. WIREs Comp. Stat. 3, 180–185.

 

Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L.D.’A., François, R., et al., 2019. Welcome to the Tidyverse. J. Open Source Softw. 4, 1686.

 

Wright Jr, O.R., 1969. Summary of research on the selection interview since 1964. Pers. Psychol. 22, 391–413.

 

Xu, Y.G., Yin, Z.H., Lei, F.M., Ding, W.N., Liu, R.S., Yu, Q., 1996. The status of Reeves’s pheasant and suggestions for conservation. Acta Zool. Sin. 42, 155 (In Chinese).

 

Xu, J-L., Zhang, Z-W., Zheng, G-M., Zhang, X-H., Sun, Q-H., McGowan, P., 2007. Home range and habitat use of Reeves’s pheasant Syrmaticus reevesii in the protected areas created from forest farms in the Dabie Mountains, central China. Bird Conserv. Int. 17, 319–330.

 

Xu, L.L., Yu, R.M., Lin, X.R., Zhang, B.W., Li, N., Lin, K., et al., 2021. Different rates of pollen and seed gene flow cause branch-length and geographic cytonuclear discordance within Asian butternuts. New Phytol. 232, 388–403.

 

Yu, G., Wang, L.G., Han, Y., He, Q.Y., 2012. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16, 284–287.

 

Zhang, Z.W., Ding, C.Q., Ding, P., Zheng, G.M., 2003. The current status and a conservation strategy for species of Galliformes in China. Biodivers. Sci. 11, 414–421 (In Chinese).

 

Zhang, C., Dong, S.S., Xu, J.Y., He, W.M., Yang, T.L., 2019. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35, 1786–1788.

 

Zheng, G.M., 2015. Pheasants in China. Higher Education Press, Beijing (In Chinese).

 

Zheng, G.M., Wang, Q.S., 1998. China Red Data Book of Endangered Animals (Aves). Science Press, Beijing (In Chinese).

 

Zheng, X., Levine, D., Shen, J., Gogarten, S.M., Laurie, C., Weir, B.S., 2012. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28, 3326–3328.

 

Zhou, C., Xu, J., Zhang, Z., 2015. Dramatic decline of the vulnerable Reeves’s pheasant Syrmaticus reevesii, endemic to Central China. Oryx 49, 529–534.

Avian Research
Article number: 100156
Cite this article:
Lu Q, Wang P, Chang J, et al. Population genomic data reveal low genetic diversity, divergence and local adaptation among threatened Reeves’s Pheasant (Syrmaticus reevesii). Avian Research, 2024, 15(1): 100156. https://doi.org/10.1016/j.avrs.2023.100156

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Received: 10 September 2023
Revised: 05 December 2023
Accepted: 18 December 2023
Published: 30 December 2023
© 2023 The Authors.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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