Skip to main content
SpringerLink
Log in

Next-generation sequencing, isolation and characterization of 14 microsatellite loci of Canthon cyanellus (Coleoptera: Scarabaeidae)

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

We used Illumina paired-end sequencing to isolate and characterize microsatellites of Canthon cyanellus, a Neotropical roller dung beetle, encompassing several lineages within its distribution range.

Methods and results

We examined C. cyanellus specimens collected at eight different localities in Mexico (two or three specimens per locality). We initially performed amplification tests with 16 loci, but two of which were unsuccessful. The 14 remaining microsatellites were polymorphic, with 2–16 alleles each. The expected and observed heterozygosity ranged from 0.11 to 0.76 and from 0.20 to 0.78, respectively.

Conclusions

These microsatellites will help to assess structure at the population and lineage levels, identify zones of potential hybridization between lineages, and draw a more precise geographic delimitation of C. cyanellus lineages.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The database of microsatellite genotypes created and analyzed in this study is included in the Supplementary Material 1.xlsx file that accompanies the published article. Additional data supporting the findings of this study are available, upon request, from the corresponding author.

Code availability

Not applicable.

References

  1. Favila ME, Díaz A (1996) Canthon cyanellus cyanellus LeConte (Coleoptera: Scarabaeidae) makes a nest in the field with several brood balls. Coleopt Bull 50:52–60

    Google Scholar 

  2. Favila ME (2001) Historia de vida y comportamiento de un escarabajo necrófago: Canthon cyanellus cyanellus LeConte (coleoptera: Scarabaeinae). Folia Entomológica Mex 40:245–278

    Google Scholar 

  3. Arellano L, León-Cortés JL, Ovaskainen O (2008) Patterns of abundance and movement in relation to landscape structure: a study of a common scarab (Canthon cyanellus cyanellus) in Southern Mexico. Landsc Ecol 23:69–78. https://doi.org/10.1007/s10980-007-9165-8

    Article  Google Scholar 

  4. Portela Salomão R, González-Tokman D, Dáttilo W et al (2018) Landscape structure and composition define the body condition of dung beetles (Coleoptera: Scarabaeinae) in a fragmented tropical rainforest. Ecol Indic 88:144–151. https://doi.org/10.1016/j.ecolind.2018.01.033

    Article  Google Scholar 

  5. Robinson M (1948) A review of the species of Canthon inhabiting the United States (Scarabaeidae: Coleoptera). Trans Am Entomol Soc 1890–74:83–100

    Google Scholar 

  6. Solís-Blanco A, Kohlmann B (2002) El género Canthon (Coleoptera: Scarabaeidae) en Costa Rica. G Ital Entomol 10:1–68

    Google Scholar 

  7. Halffter-Salas G (1961) Monografía de las especies norteamericanas del género Canthon Hoffsg. (Coleoptera: Scarabaeidae). Univ Zulia 20:225–320

    Google Scholar 

  8. Blackwelder RE (1944) Checklist of the coleopterous insects of Mexico, Central America, the West Indies, and South America. US Government Printing Office, Washington

    Google Scholar 

  9. Bellés X, Favila M (1983) Protection chimique du nid chez Canthon cyanellus cyanellus LeConte [Col. Scarabaeidae]. Bull Société Entomol Fr 88:602–607

    Google Scholar 

  10. Cortez V, Favila ME, Verdú JR, Ortiz AJ (2012) Behavioral and antennal electrophysiological responses of a predator ant to the pygidial gland secretions of two species of neotropical dung roller beetles. Chemoecology 22:29–38

    Article  CAS  Google Scholar 

  11. Cortez V, Verdú JR, Ortiz AJ et al (2015) Chemical diversity and potential biological functions of the pygidial gland secretions in two species of Neotropical dung roller beetles. Chemoecology 25:201–213. https://doi.org/10.1007/s00049-015-0189-2

    Article  CAS  Google Scholar 

  12. Favila M, Chamorro-Florescano I (2008) Male reproductive status affects contest outcome during nidification in Canthon cyanellus cyanellus LeConte (Coleoptera: scarabaeidae). Behaviour 145:1811–1821. https://doi.org/10.1163/156853908786279637

    Article  Google Scholar 

  13. Favila M, Chamorro-Florescano I (2009) The reproductive status of both sexes affects the frequency of mating and the reproductive success of males in the ball roller beetle Canthon cyanellus cyanellus (coleoptera: Scarabaeidae). Behaviour 146:1499–1512. https://doi.org/10.1163/156853909X445560

    Article  Google Scholar 

  14. Chamorro-Florescano IA, Favila ME, Macías-Ordóñez R (2011) Ownership, size and reproductive status affect the outcome of food ball contests in a dung roller beetle: when do enemies share? Evol Ecol 25:277–289

    Article  Google Scholar 

  15. Chamorro-Florescano IA, Favila ME (2016) Male success in intrasexual contests extends to the level of sperm competition in a species of dung roller beetle. Ethology 122:53–60. https://doi.org/10.1111/eth.12443

    Article  Google Scholar 

  16. Chamorro-Florescano IA, Favila ME, Macías-Ordóñez R (2017) Contests over reproductive resources in female roller beetles: outcome predictors and sharing as an option. PLoS ONE 12:e0182931. https://doi.org/10.1371/journal.pone.0182931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Favila ME, Ortiz-Domínguez M, Chamorro-Florescano I, Cortez-Gallardo V (2012) Comunicación química y comportamiento reproductor de los escarabajos rodadores del estiércol (Scarabaeinae: Scarabaeini): aspectos ecológicos y evolutivos, y sus posibles aplicaciones [pp. 141–164]. Temas Sel En Ecol Quím Insectos JC Rojas EA Malo Ed El Col Front Sur Tapachula Mex

  18. Favila ME, Nolasco J, Florescano IC, Equihua M (2005) Sperm competition and evidence of sperm fertilization patterns in the carrion ball-roller beetle Canthon cyanellus cyanellus LeConte (Scarabaeidae: Scarabaeinae). Behav Ecol Sociobiol 59:38. https://doi.org/10.1007/s00265-005-0006-y

    Article  Google Scholar 

  19. Ortiz-Domínguez M, Favila ME, Mendoza-López MR et al (2006) Epicuticular compounds and sexual recognition in the ball-roller scarab, Canthon cyanellus cyanellus. Entomol Exp Appl 119:23–27. https://doi.org/10.1111/j.1570-7458.2006.00388.x

    Article  Google Scholar 

  20. Ortíz-Domínguez M, Favila ME, Mendoza-López MR (2006) Mate recognition differences among allopatric populations of the scarab Canthon cyanellus cyanellus (Coleoptera: Scarabaeidae). Ann Entomol Soc Am 99:1248–1256. https://doi.org/10.1603/0013-8746(2006)99[1248:MRDAAP]2.0.CO;2

    Article  Google Scholar 

  21. Ortiz-Domínguez M, Favila-Castillo ME, González D, Zuñiga D (2010) Genetic differences in populations of the ball roller scarab Canthon cyanellus cyanellus (coleoptera: Scarabaeidae): a preliminary analysis. Elytron 24:99–106

    Google Scholar 

  22. Chung H, Carroll SB (2015) Wax, sex and the origin of species: dual roles of insect cuticular hydrocarbons in adaptation and mating. BioEssays 37:822–830. https://doi.org/10.1002/bies.201500014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nolasco-Soto J, González-Astorga J, Espinosa Monteros A et al (2017) Phylogeographic structure of Canthon cyanellus (coleoptera: Scarabaeidae), a Neotropical dung beetle in the Mexican transition Zone: insights on its origin and the impacts of pleistocene climatic fluctuations on population dynamics. Mol Phylogenet Evol 109:180–190. https://doi.org/10.1016/j.ympev.2017.01.004

    Article  PubMed  Google Scholar 

  24. Nolasco-Soto J, Favila ME, De Los E, Monteros A et al (2020) Variations in genetic structure and male genitalia suggest recent lineage diversification in the neotropical dung beetle complex Canthon cyanellus (Scarabaeidae: Scarabaeinae). Biol J Linn Soc 131:505–520. https://doi.org/10.1093/biolinnean/blaa131

    Article  Google Scholar 

  25. Ratnasingham S, Hebert PDN (2013) A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS ONE 8:e66213. https://doi.org/10.1371/journal.pone.0066213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Vieira MLC, Santini L, Diniz AL et al (2016) Microsatellite markers: what they mean and why they are so useful. Genet Mol Biol 39:312–328. https://doi.org/10.1590/1678-4685-GMB-2016-0027

    Article  PubMed  PubMed Central  Google Scholar 

  27. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics Babraham Institute, Cambridge, United Kingdom

    Google Scholar 

  28. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17:10–12. https://doi.org/10.14806/ej.17.1.200

    Article  Google Scholar 

  29. Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Meglécz E, Pech N, Gilles A et al (2014) QDD version 3.1: a user-friendly computer program for microsatellite selection and primer design revisited: experimental validation of variables determining genotyping success rate. Mol Ecol Resour 14:1302–1313. https://doi.org/10.1111/1755-0998.12271

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  32. Guichoux E, Lagache L, Wagner S et al (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11:591–611. https://doi.org/10.1111/j.1755-0998.2011.03014.x

    Article  CAS  PubMed  Google Scholar 

  33. Peakall R, Smouse PE (2006) genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  34. Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129. https://doi.org/10.1093/bioinformatics/bti282

    Article  CAS  PubMed  Google Scholar 

  35. Valière N (2002) gimlet: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379. https://doi.org/10.1046/j.1471-8286.2002.00228.x-i2

    Article  Google Scholar 

  36. Amos W, Hoffman JI, Frodsham A et al (2007) Automated binning of microsatellite alleles: problems and solutions. Mol Ecol Notes 7:10–14. https://doi.org/10.1111/j.1471-8286.2006.01560.x

    Article  CAS  Google Scholar 

  37. Li CC (1976) First course in population genetics. Boxwood, Pac Grove CA

    Google Scholar 

  38. Manjeri G, Muhamad R, Faridah QZ, Tan SG (2014) Development of single locus DNA microsatellite markers in Oryctes rhinoceros (Linnaeus) using 5′ anchored RAMs-PCR method. J Genet 93:92–96. https://doi.org/10.1007/s12041-012-0189-8

    Article  Google Scholar 

  39. Behura SK, Severson DW (2015) Motif mismatches in microsatellites: insights from genome-wide investigation among 20 insect species. DNA Res 22:29–38. https://doi.org/10.1093/dnares/dsu036

    Article  CAS  PubMed  Google Scholar 

  40. Song X, Yang T, Yan X et al (2020) Comparison of microsatellite distribution patterns in twenty-nine beetle genomes. Gene 757:144919. https://doi.org/10.1016/j.gene.2020.144919

    Article  CAS  PubMed  Google Scholar 

  41. Santana QC, Coetzee MPA, Steenkamp ET et al (2009) Microsatellite discovery by deep sequencing of enriched genomic libraries. Biotechniques 46:217–223. https://doi.org/10.2144/000113085

    Article  CAS  PubMed  Google Scholar 

  42. Katti MV, Ranjekar PK, Gupta VS (2001) Differential distribution of simple sequence repeats in eukaryotic genome sequences. Mol Biol Evol 18:1161–1167. https://doi.org/10.1093/oxfordjournals.molbev.a003903

    Article  CAS  PubMed  Google Scholar 

  43. Tóth G, Gáspári Z, Jurka J (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res 10:967–981. https://doi.org/10.1101/gr.10.7.967

    Article  PubMed  PubMed Central  Google Scholar 

  44. Eder MLR, Rosa AL (2020) Non-tandem repeat polymorphisms at microsatellite loci in wine yeast species. Mol Genet Genomics 295:685–693. https://doi.org/10.1007/s00438-020-01652-2

    Article  CAS  Google Scholar 

  45. Sampaio P, Correia A, Gusmão L et al (2007) Sequence analysis reveals complex mutational processes for allele length variation at two polymorphic microsatellite loci in Candida albicans. Communicating current research and educational topics and trends in applied microbiology. Formatex, Badajoz, pp 926–935

    Google Scholar 

  46. Angers B, Bernatchez L (1997) Complex evolution of a salmonid microsatellite locus and its consequences in inferring allelic divergence from size information. Mol Biol Evol 14:230–238. https://doi.org/10.1093/oxfordjournals.molbev.a025759

    Article  CAS  PubMed  Google Scholar 

  47. Schlötterer C, Zangerl B (1999) The use of imperfect microsatellites for DNA fingerprinting and population genetics. In: Epplen JT, Lubjuhn T (eds) DNA profiling and DNA fingerprinting. Birkhäuser, Basel, pp 153–165

    Chapter  Google Scholar 

  48. Viard F, Franck P, Dubois M-P et al (1998) Variation of microsatellite size homoplasy across electromorphs, loci, and populations in three invertebrate species. J Mol Evol 47:42–51

    Article  CAS  PubMed  Google Scholar 

  49. Von Wahlund S (1928) Zusammensetzung von population und Korrelationsers cheimungen von Standpunkt der veierbungs lehreaus betachlet. Hereditas 11:65–106

    Article  Google Scholar 

Download references

Acknowledgements

Sequencing was performed at the Genomics Core Facility of Servicio Central de Soporte a la Investigación Experimental (SCSIE), Universidad de Valencia. This study was funded by a research grant (CB 282922) from Consejo Nacional de Ciencia y Tecnología (CONACyT) awarded to Rosa Ana Sánchez Guillén. María Elena Sánchez-Salazar edited the English manuscript.

Funding

This study was funded by a research grant from Consejo Nacional de Ciencia y Tecnología (CONACyT) awarded to Rosa Ana Sánchez Guillén (CB 282922).

Author information

Authors and Affiliations

  1. Instituto de Ecología, A.C. Red de Biología Evolutiva, Xalapa, Veracruz, Mexico

    Luis Rodrigo Arce-Valdés, Rosa Ana Sánchez-Guillén & Janet Nolasco-Soto

  2. Instituto de Ecología, A.C. Red de Ecoetología, Xalapa, Veracruz, Mexico

    Mario E. Favila

Authors
  1. Luis Rodrigo Arce-Valdés
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rosa Ana Sánchez-Guillén
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Janet Nolasco-Soto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mario E. Favila
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All the authors contributed to the conception and design of this study. Samples were collected by JN-S. Wet lab techniques were performed by JN-S and LRA-V. Data analyses were carried out by RAS-G and LRA-V. The manuscript was written and edited equally by all the authors. All the authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Mario E. Favila.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest that are relevant to the content of this article.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Neither the article nor portions of it have been previously published elsewhere. The manuscript is not under consideration for publication in any other journal and will not be submitted elsewhere until the Molecular Biology Reports editorial process is completed. All authors consent to the publication of the manuscript in Molecular Biology Reports should the article be accepted.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 12 kb) Microsatellite genotypes database after binning

Supplementary file2 (TIFF 2080 kb) Map of C. cyanellus Mexican localities sampled in this study

11033_2021_6761_MOESM3_ESM.pdf

Supplementary file3 (PDF 362 kb) Sequence, primers, and issues found with the unsuccessfully genotyped microsatellite loci Ccy15 and Ccy16

11033_2021_6761_MOESM4_ESM.tiff

Supplementary file4 (TIFF 201 kb) Binning of the Ccy09 and Ccy12 alleles. Solid colors denote raw fragment lengths binned together into a single allele class

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arce-Valdés, L.R., Sánchez-Guillén, R.A., Nolasco-Soto, J. et al. Next-generation sequencing, isolation and characterization of 14 microsatellite loci of Canthon cyanellus (Coleoptera: Scarabaeidae). Mol Biol Rep 48, 7433–7441 (2021). https://doi.org/10.1007/s11033-021-06761-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-021-06761-8

Keywords

Search

Navigation