Skip to main content
Log in

Genital morphology and allometry differ by species and sex in Malawi cichlid fishes

  • ADVANCES IN CICHLID RESEARCH II
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The African cichlid fishes show great diversity in mating displays and reproductive strategies, yet species differences in genital morphology have been little studied. Observational notes have described broad sex differences in external genital shape between males and females, but these differences have not been quantified. We examined three aspects of genital morphology (relative anogenital distance, relative vent length, and relative external genital area) in two riverine and eleven Lake Malawi African cichlid species from eight genera. We find the most sexually distinct morphology in the Lake Malawi rock cichlids and the least sexual dimorphism in the riverine outgroup; additionally, diversity in metrics within genus indicates that these traits are recently evolving. Sexual dimorphism in morphology is present in most species, and, in the Lake Malawi species, multivariate discriminant analysis allows for accurate assignment of gonadal sex based on genital morphology and body size. This will serve as a useful method for sexing fish in a nonlethal fashion and provides a starting point for further examination of the evolution of genital morphology in this diverse group of fishes.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson, C. M. & R. B. Langerhans, 2015. Origins of female genital diversity: predation risk and lock-and-key explain rapid divergence during an adaptive radiation. Evolution 69: 2452–2467.

    Article  PubMed  Google Scholar 

  • Barlow, G. W., 2000. The Cichlid Fishes: Nature’s Grand Experiment in Evolution. Perseus Publishing, Cambridge.

    Google Scholar 

  • Brawand, D., C. E. Wagner, Y. I. Li, M. Malinsky, I. Keller, S. Fan, O. Simakov, A. Y. Ng, Z. W. Lim, E. Bezault, J. Turner-Maier, J. Johnson, R. Alcazar, H. J. Noh, P. Russell, B. Aken, J. Alfoldi, C. Amemiya, N. Azzouzi, J.-F. Baroiller, F. Barloy-Hubler, A. Berlin, R. Bloomquist, K. L. Carleton, M. A. Conte, H. D’Cotta, O. Eshel, L. Gaffney, F. Galibert, H. F. Gante, S. Gnerre, L. Greuter, R. Guyon, N. S. Haddad, W. Haerty, R. M. Harris, H. A. Hofmann, T. Hourlier, G. Hulata, D. B. Jaffe, M. Lara, A. P. Lee, I. MacCallum, S. Mwaiko, M. Nikaido, H. Nishihara, C. Ozouf-Costaz, D. J. Penman, D. Przybylski, M. Rakotomanga, S. C. P. Renn, F. J. Ribeiro, M. Ron, W. Salzburger, L. Sanchez-Pulido, M. E. Santos, S. Searle, T. Sharpe, R. Swofford, F. J. Tan, L. Williams, S. Young, S. Yin, N. Okada, T. D. Kocher, E. A. Miska, E. S. Lander, B. Venkatesh, R. D. Fernald, A. Meyer, C. P. Ponting, J. T. Streelman, K. Lindblad-Toh, O. Seehausen & F. Di Palma, 2014. The genomic substrate for adaptive radiation in African cichlid fish. Nature 513: 375–381.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brennan, P. L. R. & R. O. Prum, 2016. Mechanisms and evidence of genital coevolution: the roles of natural selection, mate choice, and sexual conflict. In Rice, W. & S. Gavrilets (eds), The Genetics and Biology of Sexual Conflict. Cold Spring Harbor Laboratory Press, New York: 385–405.

    Google Scholar 

  • Campos-Mendoza, A., B. J. McAndrew, K. Coward & N. Bromage, 2004. Reproductive response of Nile tilapia (Oreochromis niloticus) to photoperiodic manipulation; effects on spawning periodicity, fecundity and egg size. Aquaculture 231: 299–314.

    Article  Google Scholar 

  • Chervinski, J., 1983. Sexual dimorphism in tilapias. Aquaculture 35: 171–172.

    Article  Google Scholar 

  • Coleman, R. M. & A. P. Galvani, 1998. Egg size determines offspring size in neotropical cichlid fishes (Teleostei: Cichlidae). Copeia 1998: 209–213.

    Article  Google Scholar 

  • Couldridge, V. C. K., 2002. Experimental manipulation of male egg spots demonstrates female preference for one large spot in Pseudotropheus lombardoi. Journal of Fish Biology 60: 726–730.

    Google Scholar 

  • Ding, B., D. W. Daugherty, M. Husemann, M. Chen, A. E. Howe & P. D. Danley, 2014. Quantitative genetic analyses of male color pattern and female mate choice in a pair of cichlid fishes of Lake Malawi, East Africa. PLoS One 9: e114798.

    Article  PubMed  PubMed Central  Google Scholar 

  • Duponchelle, F., E. Paradis, A. J. Ribbink & G. F. Turner, 2008. Parallel life history evolution in mouthbrooding cichlids from the African Great Lakes. Proceedings of the National Academy of Sciences of the United States of America 105: 15475–15480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans, J. P., C. Gasparini, G. I. Holwell, I. W. Ramnarine, T. E. Pitcher & A. Pilastro, 2011. Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification. Proceedings of the Royal Society B: Biological Sciences 278: 2611–2620.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernald, R. D., 1977. Quantitative behavioral observations of Haplochromis burtoni under semi-natural conditions. Animal Behavior 25: 643–653.

    Article  Google Scholar 

  • Fernald, R. D. & N. R. Hirata, 1977. Field study of Haplochromis burtoni: habitats and co-habitant. Environmental Biology of Fishes 2: 299–308.

    Article  Google Scholar 

  • Ferreira, F., M. M. Santos, M. A. Reis-Henriques, N. M. Vieira & N. M. Monteiro, 2010. Sexing blennies using genital papilla morphology or ano-genital distance. Journal of Fish Biology 77: 1432–1438.

    Article  CAS  PubMed  Google Scholar 

  • Fryer, G. & T. D. Iles, 1972. The Cichlid Fishes of the Great Lakes of Africa. T.F.H. Publications, Neptune City.

    Google Scholar 

  • Getinet, G. T., 2008. Effects of maternal age on fecundity, spawning interval, and egg quality of Nile Tilapia, Oreochromis niloticus. Journal of the World Aquaculture Society 39: 671–677.

    Article  Google Scholar 

  • Guerrero III, R. D. & W. L. Shelton, 1974. An aceto-carmine squash method for sexing juvenile fishes. The Progressive Fish-Culturist 36: 56.

    Article  Google Scholar 

  • Hale, E. A., J. R. Stauffer Jr. & D. M. Megan, 1998. Exceptions to color being a sexually dimorphic character in Melanochromis auratus (Teleostei:Cichlidae). Ichthyological Exploration of Freshwaters 9: 263–266.

    Google Scholar 

  • Heinen-Kay, J. L. & R. B. Langerhans, 2013. Predation-associated divergence of male genital morphology in a livebearing fish. Journal of Evolutionary Biology 26: 2135–2146.

    Article  CAS  PubMed  Google Scholar 

  • Hert, E., 1991. Female choice based on egg-spots in Pseudotropheus aurora Burgess 1976, a rock-dwelling cichlid of Lake Malawi, Africa. Journal of Fish Biology 38: 951–953.

    Article  Google Scholar 

  • Joyce, D. A., D. H. Lunt, M. J. Genner, G. F. Turner, R. Bills & O. Seehausen, 2011. Repeated colonization and hybridization in Lake Malawi cichlids. Current Biology 21: R108–R109.

    Article  CAS  PubMed  Google Scholar 

  • Kocher, T. D., 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5: 288–298.

    Article  CAS  PubMed  Google Scholar 

  • Kolm, N., N. B. Goodwin, S. Balshine & J. D. Reynolds, 2006. Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size. Journal of Evolutionary Biology 19: 76–84.

    Article  CAS  PubMed  Google Scholar 

  • Konings, A. F., 2007. Malawi Cichlids in Their Natural Habitat. Cichlid Press, El Paso.

    Google Scholar 

  • Langerhans, R. B., C. A. Layman & T. J. DeWitt, 2005. Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species. Proceedings of the National Academy of Sciences 102: 7618–7623.

    Article  CAS  Google Scholar 

  • Malinsky, M., R. J. Challis, A. M. Tyers, S. Schiffels, Y. Terai, B. P. Ngatunga, E. A. Miska, R. Durbin, M. J. Genner & G. F. Turner, 2015. Genomic islands of speciation separate cichlid ectomorphs in an East African crater lake. Science 350: 1493–1498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin, Z. P. & L. M. Page, 2015. Comparative morphology and evolution of genital papillae in a genus of darters (Percidae: Etheostoma). Copeia 2015: 99–124.

    Article  Google Scholar 

  • Nichols, P., M. J. Genner, C. van Oosterhout, A. Smith, P. Parsons, H. Sungani, J. Swanstrom & D. A. Joyce, 2014. Secondary contact seeds phenotypic novelty in cichlid fishes. Proceedings of the Royal Society B: Biological Sciences 282: 20142272.

    Article  Google Scholar 

  • Ribbink, A. J., B. A. Marsh, A. C. Marsh, A. C. Ribbink & B. J. Sharp, 1983. A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. South African Journal of Zoology 3: 149–310.

    Article  Google Scholar 

  • Schneider, C. A., W. S. Rasband & K. W. Eliceiri, 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675.

    Article  CAS  PubMed  Google Scholar 

  • Theis, A., W. Salzburger & B. Egger, 2012. The function of anal fin egg-spots in the cichlid fish Astatotilapia burtoni. PLoS One 7: e29878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Theis, A., T. Bosia, T. Roth, W. Salzburger & B. Egger, 2015. Egg-spot pattern and body size asymmetries influence male aggression in haplochromine cichlid fishes. Behavioral Ecology 26: 1512–1519.

    Article  Google Scholar 

  • Trewavas, E., 1983. Tilapiine Fishes of the Genera Sarotherodon, Oreochromis, and Danakilia. British Museum (Natural History). Cornell University Press, New York.

    Book  Google Scholar 

  • Wickler, W., 1965. Signal value of the genital tassel in the male Tilapia macrochir Blgr. (Pisces: Chichlidae). Nature 208: 595–596.

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the North Carolina State University and the WM Keck Center for Behavioral Biology for funding; David M. Reif for statistical consultation and comments; and M. Kaitlyn Stanley and Natalie B. Roberts for assistance with photography.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emily C. Moore.

Additional information

Guest editors: S. Koblmüller, R. C. Albertson, M. J. Genner, K. M. Sefc & T. Takahashi / Advances in Cichlid Research II: Behavior, Ecology and Evolutionary Biology

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

10750_2016_2912_MOESM2_ESM.eps

Online Resource. 1 Raw measurements (in pixels) of anus area and external genital area by standard length (mm) for four Lake Malawi species. A linear relationship is present between standard length and raw genital area (b) for both sexes, but not for standard length and raw anus area (a) (EPS 1088 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moore, E.C., Roberts, R.B. Genital morphology and allometry differ by species and sex in Malawi cichlid fishes. Hydrobiologia 791, 127–143 (2017). https://doi.org/10.1007/s10750-016-2912-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2912-6

Keywords

Navigation