AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Avian Research Article
PDF (1.9 MB)
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Development and parentage analysis of SNP markers for Chestnut-vented Nuthatch (Sitta nagaensis) based on ddRAD-seq data

Qingmiao Yuana,d, Xi Lub,d, Ruixin Moc,d, Xianyin Xue, Xu Luoa( ), Yubao Duana,d( )
Key Laboratory for Conserving Wildlife with Small Populations in Yunnan, Southwest Forestry University, Kunming 650224, China
Key Laboratory for Forest Resources Conservation and Utilization in the Southwest Mountains of China, Ministry of Education, Southwest Forestry University, Kunming 650224, China
Key Laboratory of Forest Disaster Warning and Control of Yunnan Province, Southwest Forestry University, Kunming 650224, China
College of Forestry, Southwest Forestry University, Kunming 650224, China
Administration of Zixi Mountain Provincial Nature Reserve, Chuxiong 675008, China
Show Author Information

Abstract

Extra-pair paternity (EPP) is commonly found in socially monogamous birds, especially in small passerine birds, and there are interspecific and intraspecific variations in the extent of EPP. The Chestnut-vented Nuthatch (Sitta nagaensis) is a socially monogamous passerine bird, and verifying whether this species has EPP relies on parentage testing—S. nagaensis is not known to have EPP. In this study, we developed SNP markers of this species that are informative for parentage analysis from double digest restriction site-associated DNA sequencing (ddRAD-seq) data. A panel consisting of 50 SNP markers, with a mean heterozygosity of 0.343, was used to resolve 95% of nestlings to fathers. The combined exclusion probabilities for the first parent and second parent were 0.991 and 0.9999, respectively. This panel of SNP markers is a powerful tool for parentage assignments in S. nagaensis. In addition, we found that three offspring (7.9%) from three nests (23.1%) were the result of extra-pair fertilization out of 38 offspring in 13 nests. Our study provided information on parentage analysis that has not been reported before in S. nagaensis. It also supplemented the understudied EPP behavior of birds in Asia, contributing to a general understanding of the EPP behaviors of birds.

Keywords

Extra-pair paternitySNPsChestnut-vented NuthatchddRAD sequencingParentage analysis

References

 

Anderson, E.C., Garza, J.C., 2006. The power of single-nucleotide polymorphisms for large-scale parentage inference. Genetics 172, 2567–2582.
Crossref Google Scholar
 

Arrieta, R.S., Campagna, L., Mahler, B., Llambías, P.E., 2022. Neither paternity loss nor perceived threat of cuckoldry affects male nestling provisioning in grass wrens. Behav. Ecol. Sociobiol. 76, 147.
Crossref Google Scholar
 

Baird, N.A., Etter, P.D., Atwood, T.S., Currey, M.C., Shiver, A.L., Lewis, Z.A., et al., 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3, e3376.
Crossref Google Scholar
 

Baruch, E., Weller, J.I., 2008. Estimation of the number of SNP genetic markers required for parentage verification. Anim. Genet. 39, 474–479.
Crossref Google Scholar
 

Birkhead, T., 1987. Sperm competition in birds. Trends Ecol. Evol. 2, 268–272.
Crossref Google Scholar
 

Brouwer, L., Griffith, S.C., 2019. Extra-pair paternity in birds. Mol. Ecol. 2, 4864–4882.
Crossref Google Scholar
 

Brumfield, R.T., Beerli, P., Nickerson, D.A., Edwards, S.V., 2003. The utility of single nucleotide polymorphisms in inferences of population history. Trends Ecol. Evol. 18, 249–256.
Crossref Google Scholar
 

Campagna, L., Gronau, I., Silveira, L.F., Siepel, A., Lovette, I.J., 2015. Distinguishing noise from signal in patterns of genomic divergence in a highly polymorphic avian radiation. Mol. Ecol. 24, 4238–4251.
Crossref Google Scholar
 

Catchen, J., Hohenlohe, P.A., Bassham, S., Amores, A., Cresko, W.A., 2013. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140.
Crossref Google Scholar
 

Cramer, E.R.A., Hall, M.L., de Kort, S.R., Lovette, I.J., Vehrencamp, S.L., 2011. Infrequent extra-pair paternity in the Banded Wren, a synchronously breeding tropical passerine. Condor 113, 637–645.
Crossref Google Scholar
 

Cockburn, A., 2006. Prevalence of different modes of parental care in birds. P Roy Soc B-Biol Sci 273, 1375–1383.
Crossref Google Scholar
 

Coleman, S.W., Jones, A.G., 2011. Patterns of multiple paternity and maternity in fishes. Biol. J. Linn. Soc. 103, 735–760.
Crossref Google Scholar
 

Cousseau, L., Van de Loock, D., Githiru, M., Vangestel, C., Lens, L., 2020. Female need for paternal care shapes variation in extra-pair paternity in a cooperative breeder. Behav. Ecol. 31, 548–558.
Crossref Google Scholar
 

Dawson, D.A., Ball, A.D., Spurgin, L.G., Martín-Gálvez, D., Stewart, I.R.K., Horsburgh, G. J., et al., 2013. High-utility conserved avian microsatellite markers enable parentage and population studies across a wide range of species. BMC Genom. 14, 176–197.
Crossref Google Scholar
 

DeWoody, J.A., Avise, J.C., 2000. Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J. Fish. Biol. 56, 461–473.
Crossref Google Scholar
 

Dussault, F.M., Boulding, E.G., 2018. Effect of minor allele frequency on the number of single nucleotide polymorphisms needed for accurate parentage assignment: a methodology illustrated using Atlantic salmon. Aquacult. Res. 49, 1368–1372.
Crossref Google Scholar
 

Ellegren, H., 2004. Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5, 435–445.
Crossref Google Scholar
 

Feng, Y.Y., Li, Q.S., Liang, D., Jiang, D.M., Wu, X.R., Gao, G., et al., 2019. Annual variation of bird richness in winter in Zixi Mountain, Yunnan Province. Journal of Southwest Forestry University 39, 110–115 (In Chinese with English Abstract).
Google Scholar
 

Flanagan, S.P., Jones, A.G., 2019. The future of parentage analysis: from microsatellites to SNPs and beyond. Mol. Ecol. 28, 544–567.
Crossref Google Scholar
 

Glaubitz, J.C., Rhodes, O.E., Dewoody, J.A., 2003. Prospects for inferring pairwise relationships with single nucleotide polymorphisms. Mol. Ecol. 12, 1039–1047.
Crossref Google Scholar
 

Griffith, S.C., Owens, I.P., Thuman, K.A., 2002. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11, 2195–2212.
Crossref Google Scholar
 

Gudex, B., Walker, M., Fisher, P., Spelman, R., 2014. Validation of a single-nucleotide polymorphism panel for parentage testing of farmed red deer. Anim. Genet. 45, 142–143.
Crossref Google Scholar
 

Gutierrez, A.P., Turner, F., Gharbi, K., Talbot, R., Lowe, N.R., Peñaloza, C., et al., 2017. Development of a medium density combined-species SNP array for Pacific and European oysters (Crassostrea gigas & Ostrea edulis). G3-Genes Genom Genet. 7, 2209–2218.
Crossref Google Scholar
 

Han, K.L., Cox, J.A., Kimball, R.T., 2015. Uncommon levels of relatedness and parentage in a cooperatively breeding bird, the Brown-Headed Nuthatch (Sitta pusilla). Wilson J. Ornithol. 127, 593–600.
Crossref Google Scholar
 

Jetz, W., Rubenstein, D.R., 2011. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr. Biol. 21, 72–78.
Crossref Google Scholar
 

John, M.J.N., Karen, P., He, F.Q., 2000. Field Handbook of Chinese Birds. Hunan Education Publishing House, Changsha, China.
 

Kaiser, S.A., Taylor, S.A., Chen, N., Sillett, T.S., Bondra, E.R., Webster, M.S., 2017. A comparative assessment of SNP and microsatellite markers for assigning parentage in a socially monogamous bird. Mol. Ecol. Resour. 17, 183–193.
Crossref Google Scholar
 

Kalinowski, S.T., Taper, M.L., Marshall, T.C., 2007. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106.
Crossref Google Scholar
 

Kess, T., Gross, J., Harper, F., Boulding, E.G., 2016. Low-cost ddRAD method of SNP discovery and genotyping applied to the periwinkle Littorina saxatilis. J. Molluscan Stud. 82, 104–109.
Crossref Google Scholar
 
Lalitha, S., 2000. Primer Premier 5, vol. 1. Biotech Software & Internet Report, pp. 270–272.
Crossref
 

Lecce, I.D., Perrier, C., Szulkin, M., Sudyka, J., 2023. Extra-pair paternity, breeding density, and synchrony in natural cavities versus nestboxes in two passerine birds. Ecol. Evol. 13, e10163.
Crossref Google Scholar
 

Liu, S.X., Palti, Y., Gao, G.T., Rexroad, C.E., 2015. Development and validation of a SNP panel for parentage assignment in rainbow trout. Aquaculture 452, 178–182.
Crossref Google Scholar
 

Marshall, T.C., Slate, J., Kruuk, L.E., Pemberton, J.M., 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639–655.
Crossref Google Scholar
 

Miller, J.M., Campbell, E.O., Rotella, J.J., Macdonald, K.R., Gelatt, T.S., Davis, C.S., 2022. Evaluation of novel genomic markers for pedigree construction in an isolated population of Weddell Seals (Leptonychotes weddellii) at White Island, Antarctica. Conserv. Genet. Resour. 14, 69–80.
Crossref Google Scholar
 

Mo, R.X., Li, Y., Yuan, Q.M., He, M.Y., Xu, X.Y., Chen, G.J., et al., 2023. Nest-site features and breeding ecology of chestnut-vented nuthatch Sitta nagaensis in southwestern China. Animals 13, 2034.
Crossref Google Scholar
 

Morin, P.A., Luikart, G., Wayne, R.K., 2004. SNPs in ecology, evolution and conservation. Trends Ecol. Evol. 19, 208–216.
Crossref Google Scholar
 

Nielsen, R., Paul, J.S., Albrechtsen, A., Song, Y.S., 2011. Genotype and SNP calling from next-generation sequencing data. Nat. Rev. Genet. 12, 443–451.
Crossref Google Scholar
 

Peterson, B.K., Weber, J.N., Kay, E.H., Fisher, H.S., Hoekstra, H.E., 2012. Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7, e37135.
Crossref Google Scholar
 

Pompanon, F., Bonin, A., Bellemain, E., Taberlet, P., 2005. Genotyping errors: causes, consequences and solutions. Nat. Rev. Genet. 6, 847–859.
Crossref Google Scholar
 

Potti, J., Camacho, C., Canal, D., Martínez-Padilla, J., 2021. Three decades of crimes and misdemeanours in the nest box life of European Pied Flycatchers Ficedula hypoleuca. ARDEOLA 68, 315–333.
Crossref Google Scholar
 

Premachandra, H.K.A., Nguyen, N.H., Knibb, W., 2019. Effectiveness of SNPs for parentage and sibship assessment in polygamous yellowtail kingfish Seriola lalandi. Aquaculture 499, 24–31.
Crossref Google Scholar
 

Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A.R., Bender, D., et al., 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575.
Crossref Google Scholar
 

Reitsma, L.R., Jukosky, J.A., Kimiatek, A.J., Goodnow, M.L., Hallworth, M.T., 2018. Extra-pair paternity in a long-distance migratory songbird beyond neighbors' borders and across male age classes. Can. J. Zool. 96, 49–54.
Crossref Google Scholar
 

Segelbacher, G., Kabisch, D., Stauss, M., Tomiuk, J., 2005. Extra-pair young despite strong pair bonds in the European Nuthatch (Sitta europaea). J. Ornithol. 146, 99–102.
Crossref Google Scholar
 

Strucken, E.M., Lee, S.H., Lee, H.K., Song, K.D., Gibson, J.P., Gondro, C., 2016. How many markers are enough? Factors influencing parentage testing in different livestock populations. J. Anim. Breed. Genet. 133, 13–23.
Crossref Google Scholar
 

Thrasher, D.J., Butcher, B.G., Campagna, L., Webster, M.S., Lovette, I.J., 2018. Doubledigest RAD sequencing outperforms microsatellite loci at assigning paternity and estimating relatedness: a proof of concept in a highly promiscuous bird. Mol Ecol Resour 18, 953–965.
Crossref Google Scholar
 

Toews, D.P.L., Campagna, L., Taylor, S.A., Balakrishnan, C.N., Baldassarre, D.T., DeaneCoe, P.E., et al., 2015. Genomic approaches to understanding population divergence and speciation in birds. Auk 133, 13–30.
Crossref Google Scholar
 

Uller, T., Olsson, M., 2008. Multiple paternity in reptiles: patterns and processes. Mol. Ecol. 17, 2566–2580.
Crossref Google Scholar
 

Valenzuela-Guerra, P., Morales-Moraga, D., González-Acuña, D., Vianna, J.A., 2013. Geographic morphological variation of Gentoo penguin (Pygoscelis papua) and sex identification: using morphometric characters and molecular markers. Polar Biol. 36, 1723–1734.
Crossref Google Scholar
 

Vignal, A., Milan, D., SanCristobal, M., Eggen, A., 2002. A review on SNP and other types of molecular markers and their use in animal genetics. Genet. Sel. Evol. 34, 275–306.
Crossref Google Scholar
 

Wan, D.M., Chang, P., Yin, J.X., 2013. Causes of extra-pair paternity and its inter-specific variation in socially monogamous birds. Acta Ecol. Sin. 33, 158–166.
Crossref Google Scholar
 

Wang, B., Xie, X., Liu, S.M., Wang, X.J., Pang, H., Liu, Y., 2017. Development and characterization of novel microsatellite markers for the Common Pheasant (Phasianus colchicus) using RAD-seq. Avian Res. 8, 4.
Crossref Google Scholar
 

Wang, J., Wei, Y.H., Zhang, L., Jiang, Y.T., Li, K.K., Wan, D.M., 2021. High level of extrapair paternity in the socially monogamous Marsh Tits (Poecile palustris). Avian Res. 12, 69.
Crossref Google Scholar
 

Weinman, L.R., Solomon, J.W., Rubenstein, D.R., 2015. A comparison of single nucleotide polymorphism and microsatellite markers for analysis of parentage and kinship in a cooperatively breeding bird. Mol. Ecol. Resour. 15, 502–511.
Crossref Google Scholar
 

Weng, Z.Y., Yang, Y., Wang, X., Wu, L., Hua, S.J., Zhang, H.F., et al., 2021. Parentage analysis in Giant Grouper (Epinephelus lanceolatus) using microsatellite and SNP markers from genotyping-by-sequencing data. Genes 12, 1042.
Crossref Google Scholar
 

Zhang, L., Bai, L.M., Wang, J., Wan, D.M., Liang, W., 2021. Occupation rates of artificial nest boxes by secondary cavity-nesting birds: the influence of nest site characteristics. J. Nat. Conserv. 63, 12605.
Crossref Google Scholar
Avian Research
Volume 15 Issue 2,
June 2024
Article number: 100179
DOI: 10.1016/j.avrs.2024.100179
Cite this article:
Yuan Q, Lu X, Mo R, et al. Development and parentage analysis of SNP markers for Chestnut-vented Nuthatch (Sitta nagaensis) based on ddRAD-seq data. Avian Research, 2024, 15(2): 100179. https://doi.org/10.1016/j.avrs.2024.100179

101

Views

1

Downloads

0

Crossref

0

Web of Science

0

Scopus

0

CSCD

Altmetrics
Received: 07 February 2024
Revised: 25 April 2024
Accepted: 29 April 2024
Published: 06 May 2024
© 2024 The Authors.

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