Development and characterization of microsatellite markers in Rosy-faced and other lovebirds (Agapornis spp.) using next-generation sequencing

Abstract

Agapornis are a group of small African parrots that are heavily traded around the world. They are invasive species in many places, but some of them are listed as Vulnerable or Near Threatened. However, the genetic tools for assessing inter-individual relationships, population structure, and genetic diversity of these birds are very limited. Therefore, we developed polymorphic microsatellite markers in A. roseicollis and tested the transferability on 5 lovebird species including A. personatus, A. nigrigenis, A. fischeri, A. pullarius, and A. canus, and two closely related outgroups (i.e. Bolbopsittacus lunulatus and Loriculus galgulus). We first performed whole-genome re-sequencing on five individuals of A. roseicollis to identify potential polymorphic loci. Out of 37 loci tested in 11 A. roseicollis, 27 loci were demonstrated to be polymorphic, with the number of the alleles ranging from 2 to 7 (mean = 3.963). The observed heterozygosity ranged from 0 to 0.875 (mean = 0.481) and expected heterozygosity ranged from 0.233 to 0.842 (mean = 0.642). Five loci (Agro-A13, p < 0.01; Agro-A15, p < 0.05; Agro-A43, p < 0.05, Agro-A65, p < 0.05; Agro-A67, p < 0.05) were detected to deviate from Hardy-Weinberg equilibrium, with the presence of null alleles suggested in locus Agro-A13 and Agro-A77. The exclusion powers for PE1 and PE2 are 0.997 and 0.999, respectively. The 27 novel polymorphic markers developed here will be useful for parentage and kinship assignment and population genetics study in Agapornis, and provide a tool for scientific research, captive breeding industry, and invasion and conservation management of these species.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. 1.

    Dilger WC (1960) The comparative ethology of the African parrot genus Agapornis. Ethology 17:649–685. https://doi.org/10.1111/j.1439-0310.1960.tb00412.x

    Article  Google Scholar 

  2. 2.

    Mori E, Cardador L, Reino L, White RL, Hernández-Brito D, Le Louarn M, Mentil L, Edelaar P, Pârâu LG, Nikolov BP, Menchetti M (2019) Lovebirds in the air: trade patterns, establishment success and niche shifts of Agapornis parrots within their non-native range. Biol Invasions. https://doi.org/10.1007/s10530-019-02100-y

  3. 3.

    Van den Abeele D (2016) Lovebirds compendium. About Pets Publishers, The Netherlands

    Google Scholar 

  4. 4.

    IUCN (2019) The IUCN Red List of Threatened Species. Version 2019–3. http://www.iucnredlist.org. Accessed 10 Dec 2019

  5. 5.

    Ndithia H, Perrin MR (2006) Diet and foraging behaviour of the rosy-faced lovebird Agapornis roseicollis in Namibia. Ostrich 77(1–2):45–51. https://doi.org/10.2989/00306520609485507

    Article  Google Scholar 

  6. 6.

    Lever C (2005) Naturalized animals of the British Isles. T and AD Poyser Editions, London

    Google Scholar 

  7. 7.

    Menchetti M, Mori E (2014) Worldwide impact of alien parrots (Aves Psittaciformes) on native biodiversity and environment: a review. Ethol Ecol Evol 26(2–3):172–194. https://doi.org/10.1080/03949370.2014.905981

    Article  Google Scholar 

  8. 8.

    Dubois PJ, Maillard JF, Cugnasse JM (2016) Les populations d’oiseaux allochtones en France en 2015 (4e enquête nationale). Ornithos 23:129–141

    Google Scholar 

  9. 9.

    Lever C (1994) Naturalized animals: the ecology of successfully introduced species. Poyser Natural History, London

    Google Scholar 

  10. 10.

    Zwan H, Visser C, Schoonen M, Van Der Sluis R (2019) Development of an SNP -based parentage verification panel for lovebirds. Anim Genet. https://doi.org/10.1111/age.12859

  11. 11.

    Van Der Zwan H, Van Der Westhuizen F, Visser C, Van Der Sluis R (2018) Draft De novo genome sequence of Agapornis roseicollis for application in avian breeding. Anim Biotechnol 29(4):241–246. https://doi.org/10.1080/10495398.2017.1367692

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Faircloth BC (2008) Msatcommander: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol Ecol Resour 8(1):92–94. https://doi.org/10.1111/j.1471-8286.2007.01884.x

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3--new capabilities and interfaces. Nucleic Acids Res 40(15):e115–e115. https://doi.org/10.1093/nar/gks596

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18(2):233–234. https://doi.org/10.1038/72708

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv 1303

  17. 17.

    Thorvaldsdottir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief in Bioinform 14(2):178–192. https://doi.org/10.1093/bib/bbs017

    CAS  Article  Google Scholar 

  18. 18.

    Gardner MG, Fitch AJ, Bertozzi T, Lowe AJ (2011) Rise of the machines--recommendations for ecologists when using next generation sequencing for microsatellite development. Mol Ecol Resour 11(6):1093–1101. https://doi.org/10.1111/j.1755-0998.2011.03037.x

    Article  PubMed  Google Scholar 

  19. 19.

    Dawson DA, Horsburgh GJ, Küpper C, Stewart IRK, Ball AD, Durrant KL, Hansson B, Bacon I, Bird S, Klein Á, Krupa AP, Lee J-W, Martín-Gálvez D, Simeoni M, Smith G, Spurgin LG, Burke T (2010) New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility - as demonstrated for birds. Mol Ecol Resour 10(3):475–494. https://doi.org/10.1111/j.1755-0998.2009.02775.x

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Wang J (2004) Estimating pairwise relatedness from dominant genetic markers. Mol Ecol 13(10):3169–3178. https://doi.org/10.1111/j.1365-294x.2004.02298.x

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research--an update. Bioinformatics 28(19):2537–2539. https://doi.org/10.1093/bioinformatics/bts460

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and Ecumenicism. J Hered 86(3):248–249. https://doi.org/10.1093/oxfordjournals.jhered.a111573

    Article  Google Scholar 

  23. 23.

    Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x

    CAS  Article  Google Scholar 

  24. 24.

    Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16(5):1099–1106. https://doi.org/10.1111/j.1365-294x.2007.03089.x

    Article  PubMed  Google Scholar 

Download references

Funding

This research was supported by the Seed Fund for Basic Research for New Staff (HKU).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Simon Yung Wa Sin.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

All animals used in this study were approved and handled in accordance with the guidelines provided by the Committee on the Use of Live Animals in Teaching and Research (CULATR) in the Laboratory Animal Unit, HKU (CULATR Approval Number: 4749-18).

Informed consent

All authors consent to participate. All authors consent to publication.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lam, D.K., Sin, S.Y.W. Development and characterization of microsatellite markers in Rosy-faced and other lovebirds (Agapornis spp.) using next-generation sequencing. Mol Biol Rep (2020). https://doi.org/10.1007/s11033-020-05623-z

Download citation

Keywords

  • Agapornis roseicollis
  • High throughput sequencing
  • Kinship inference
  • Parentage analysis
  • Peach-faced lovebirds
  • Polymorphic microsatellite loci