Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Competition and phylogeny determine community structure in Müllerian co-mimics

Abstract

Until recently, the study of negative and antagonistic interactions (for example, competition and predation) has dominated our understanding of community structure, maintenance and assembly1. Nevertheless, a recent theoretical model suggests that positive interactions (for example, mutualisms) may counterbalance competition, facilitating long-term coexistence even among ecologically undifferentiated species2. Müllerian mimics are mutualists that share the costs of predator education3 and are therefore ideally suited for the investigation of positive and negative interactions in community dynamics. The sole empirical test of this model in a Müllerian mimetic community supports the prediction that positive interactions outweigh the negative effects of spatial overlap4 (without quantifying resource acquisition). Understanding the role of trophic niche partitioning in facilitating the evolution and stability of Müllerian mimetic communities is now of critical importance, but has yet to be formally investigated. Here we show that resource partitioning and phylogeny determine community structure and outweigh the positive effects of Müllerian mimicry in a species-rich group of neotropical catfishes. From multiple, independent reproductively isolated allopatric communities displaying convergently evolved colour patterns, 92% consist of species that do not compete for resources. Significant differences in phylogenetically conserved traits (snout morphology and body size) were consistently linked to trait-specific resource acquisition. Thus, we report the first evidence, to our knowledge, that competition for trophic resources and phylogeny are pivotal factors in the stable evolution of Müllerian mimicry rings. More generally, our work demonstrates that competition for resources is likely to have a dominant role in the structuring of communities that are simultaneously subject to the effects of both positive and negative interactions.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Phylogenetic relationships of Corydoradinae including co-mimics.
Figure 2: Geographical distribution of mimetic communities.

Accession codes

Data deposits

Sequence data have been deposited in GenBank (http://www.ncbi.nlm.nih.gov/genbank/) with accession numbers detailed in Supplementary Table 1.

References

  1. May, R. M. The role of theory in ecology. Am. Zool. 21, 903–910 (1981)

    Article  Google Scholar 

  2. Gross, K. Positive interactions among competitors can produce species-rich communities. Ecol. Lett. 11, 929–936 (2008)

    Article  Google Scholar 

  3. Rowland, H. M., Ihalainen, E., Lindström, L., Mappes, J. & Speed, M. P. Co-mimics have a mutualistic relationship despite unequal defences. Nature 448, 64–67 (2007)

    Article  ADS  CAS  Google Scholar 

  4. Elias, M., Gompert, Z., Jiggins, C. & Willmott, K. Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biol. 6, (2008)

  5. Brooker, R. W. et al. Facilitation in plant communities: the past, the present, and the future. J. Ecol. 96, 18–34 (2008)

    Article  MathSciNet  Google Scholar 

  6. Callaway, R. M. Positive interactions among plants. Bot. Rev. 61, 306–349 (1995)

    Article  Google Scholar 

  7. Stachowicz, J. J. Mutualism, facilitation, and the structure of ecological communities. Bioscience 51, 235–246 (2001)

    Article  Google Scholar 

  8. Ruxton, G. D., Sherratt, T. N. & Speed, M. P. Avoiding Attack (Oxford Univ. Press, 2004)

    Book  Google Scholar 

  9. Fuller, I. A. & Evers, H.-G. Identifying Corydoradinae Catfish (Ian Fuller Enterprises, 2005)

    Google Scholar 

  10. Nelson, J. Fishes of the World (John Wiley & Sons, 2006)

    Google Scholar 

  11. Nijssen, H. Revision of the Surinam catfishes of the genus Corydoras (Pisces; Siluriformes; Callichthyidae). Beaufortia 18, 1–75 (1970)

    Google Scholar 

  12. Sands, D. D. The Behaviour and Evolutionary Ecology of Corydoras adolfoi and Corydoras imitator: Studies on Two Species of Sympatric Catfish from the Upper Rio Negro, Brazil. PhD thesis, Univ. Liverpool. (1994)

    Google Scholar 

  13. Axenrot, T. E. & Kullander, S. O. Corydoras diphyes (Siluriformes: Callichthyidae) and Otocinclus mimulus (Siluriformes: Loricariidae), two new species of catfishes from Paraguay, a case of mimetic association. Ichthyol. Explor. Freshwat. 14, 249–272 (2003)

    Google Scholar 

  14. Luz-Agostinho, K. D. G., Agostinho, A. A., Gomes, L. C. & Julio, H. F. Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Parana River floodplain. Hydrobiologia 607, 187–198 (2008)

    Article  Google Scholar 

  15. Power, M. E. Depth distributions of armored catfish—Predator-induced resource avoidance. Ecology 65, 523–528 (1984)

    Article  Google Scholar 

  16. Greven, H., Flasbeck, T. & Passia, D. Axillary glands in the armoured catfish Corydoras aeneus (Callichthyidae, Siluriformes). Verh. Ges. Ichthyol. 6, 65–69 (2006)

    Google Scholar 

  17. Kiehl, E., Rieger, C. & Greven, H. Axillary gland secretions contribute to the stress-induced discharge of a bactericidal substance in Corydoras sterbai (Callichthyidae, Siluriformes). Verh. Ges. Ichthyol. 6, 111–115 (2006)

    Google Scholar 

  18. Wright, J. J. Diversity, phylogenetic distribution, and origins of venomous catfishes. BMC Evol. Biol. 9, 282 (2009)

    Article  Google Scholar 

  19. Müller, F. Über die vortheile der mimicry bei schmetterlingen. Zool. Anz. 1, 54–55 (1878)

    Google Scholar 

  20. Endler, J. A. & Mappes, J. Predator mixes and the conspicuousness of aposematic signals. Am. Nat. 163, 532–547 (2004)

    Article  Google Scholar 

  21. Merilaita, S. & Ruxton, G. D. Aposematic signals and the relationship between conspicuousness and distinctiveness. J. Theor. Biol. 245, 268–277 (2007)

    Article  Google Scholar 

  22. Wüster, W. et al. Do aposematism and Batesian mimicry require bright colours? A test, using European viper markings. Proc. R. Soc. Lond. B 271, 2495–2499 (2004)

    Article  Google Scholar 

  23. Wright, J. J. Conservative coevolution of Müllerian mimicry in a group of rift lake catfish. Evolution 10.1111/j.1558-5646.2010.01149.x (22 October 2010)

  24. Hinegardner, R. & Rosen, D. E. Cellular DNA content and evolution of Teleostean fishes. Am. Nat. 106, 621–644 (1972)

    Article  CAS  Google Scholar 

  25. Oliveira, C., Almeida-Toledo, L. F., Mori, L. & Toledo-Filho, S. A. Extensive chromosomal rearrangements and nuclear-DNA content changes in the evolution of the armored catfishes genus Corydoras (Pisces, Siluriformes, Callichthyidae). J. Fish Biol. 40, 419–431 (1992)

    Article  Google Scholar 

  26. Peterson, B. J. & Fry, B. Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Syst. 18, 293–320 (1987)

    Article  Google Scholar 

  27. Rubenstein, D. R. & Hobson, K. A. From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol. Evol. 19, 256–263 (2004)

    Article  Google Scholar 

  28. West, J. B., Bowen, G. J., Cerling, T. E. & Ehleringer, J. R. Stable isotopes as one of nature's ecological recorders. Trends Ecol. Evol. 21, 408–414 (2006)

    Article  Google Scholar 

  29. Clabaut, C., Bunje, P. M. E., Salzburger, W. & Meyer, A. Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations. Evolution 61, 560–578 (2007)

    Article  Google Scholar 

  30. Genner, M. J., Turner, G. F., Barker, S. & Hawkins, S. J. Niche segregation among Lake Malawi cichlid fishes? Evidence from stable isotope signatures. Ecol. Lett. 2, 185–190 (1999)

    Article  Google Scholar 

  31. Drummond, A. J. et al. Geneious. v4.7 〈http://www.geneious.com〉 (2009)

  32. Loytynoja, A. & Milinkovitch, M. C. SOAP, cleaning multiple alignments from unstable blocks. Bioinformatics 17, 573–574 (2001)

    Article  CAS  Google Scholar 

  33. Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bionf. 5, 1–19 (2004)

    Article  Google Scholar 

  34. Posada, D. jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256 (2008)

    Article  CAS  Google Scholar 

  35. Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006)

    Article  CAS  Google Scholar 

  36. Stamatakis, A., Hoover, P. & Rougemont, J. A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57, 758–771 (2008)

    Article  Google Scholar 

  37. Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)

    Article  CAS  Google Scholar 

  38. Rambaut, A. & Drummond, A. J. Tracer. v1.4 〈http://beast.bio.ed.ac.uk/Tracer〉 (2004)

  39. Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, (2007)

  40. Pinnegar, J. K. & Polunin, N. V. C. Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct. Ecol. 13, 225–231 (1999)

    Article  Google Scholar 

  41. Kovach, W. L. MVSP—A MultiVariate Statistical Package for Windows, version 3.1 (Kovach Computing Services, 1999)

  42. Bonnet, E. & Van de Peer, Y. zt: a software tool for simple and partial Mantel tests. J. Stat. Softw. 7, 1–12 (2002)

    Article  Google Scholar 

Download references

Acknowledgements

This research was funded by NERC small grant (NE/C001168/1), NERC Mass Spectrometry access grant (NE/F007205/1) awarded to M.I.T., and a NERC PhD studentship (NE/F007205/1) awarded to M.A.A. Research was also supported by UNESP, Brazil. We would like to thank the staff and students of UNESP, Botucatu, Brazil for facilities and research support during fieldwork including P. Venere for helping to collect samples in the Rio Araguaia, and M. Britto for identifying samples. We would also like to thank B. Emerson and G. Ruxton for their suggestions and critical evaluation of the manuscript. We thank J. Montoya-Burgos, M. Sabaj Perez, I. Fuller, H.-G. Evers, M. Walters and K. Mathiesen for providing tissue samples and photographs, and A. Orchard for photographing preserved specimens.

Author information

Authors and Affiliations

Authors

Contributions

M.I.T. conceived the study, contributed to all data collection, analysis and writing and supervised M.A.A.; M.A.A. conducted fieldwork, DNA sequencing, stable isotope analysis, morphology and colour pattern analysis, data analysis and writing. C.O. co-supervised M.A.A. and organized and participated in field sampling and writing. M.M. and R.A.R.M. conducted DNA sequencing and stable isotope analysis, respectively; J.N. provided stable isotope advice and guidance; and S.C. co-supervised M.A.A. and contributed to writing.

Corresponding author

Correspondence to Martin I. Taylor.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-9 with legends and Supplementary Tables 1-4. (PDF 6042 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Alexandrou, M., Oliveira, C., Maillard, M. et al. Competition and phylogeny determine community structure in Müllerian co-mimics. Nature 469, 84–88 (2011). https://doi.org/10.1038/nature09660

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09660

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing