Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Interspecific variation in relative brain size is not correlated with intensity of sexual selection in waterfowl (Anseriformes)

P.-J. Guay A C and A. N. Iwaniuk B
+ Author Affiliations
- Author Affiliations

A Department of Zoology, The University of Melbourne, Vic. 3010, Australia.

B Division of Birds, Smithsonian Institution, National Museum of Natural History, Washington, DC 20560, USA.

C Corresponding author. Email: p.guay@zoology.unimelb.edu.au

Australian Journal of Zoology 56(5) 311-321 https://doi.org/10.1071/ZO08082
Submitted: 16 October 2008  Accepted: 17 November 2008   Published: 20 February 2009

Abstract

The role of sexual selection in shaping the brain is poorly understood. Although numerous studies have investigated the role of natural selection, relatively few have focussed on the role of sexual selection. Two important factors influencing the intensity of sexual selection are sperm competition and pair bonding and three different hypotheses have been proposed to explain how they could influence relative brain size. (1) The ‘extra-pair mating’ hypothesis predicts that sexual dimorphism in brain size will increase with sperm competition intensity. (2) The ‘Machiavellian intelligence’ hypothesis predicts that brain size will be larger in species with intense sperm competition. (3) The ‘relationship intelligence’ hypothesis predicts that species forming long-term pair bonds will have larger brains. We investigated sexual dimorphism in brain size and tested these three hypotheses in waterfowl by studying correlations between relative brain volume and three measures of sperm competition (testicular mass, phallus length and mating strategy) and pair-bond duration using the modern phylogenetic comparative approach. We found no evidence of sexual dimorphism in brain size in waterfowl after controlling for body mass and found no support for any of the three hypotheses. This suggests that brain size may not be sexually selected in waterfowl, despite evidence of sexual selection pressures on other morphological characters.


Acknowledgements

This research was supported by funding from the Department of Zoology and the Faculty of Science of the University of Melbourne, the David Hay Scholarship, le Fonds québécois de la recherche sur la nature et les technologies, the Academy of Natural Sciences, Philadelphia, the Field Museum of Natural History, the American Museum of Natural History and the Smithsonian Fellowship program. We thank the following institutions for allowing access to their collection and/or logistical help: The Auckland Museum, the Australian Museum, the Bird group of the Natural History Museum at Tring, the Bishop Museum, the Canadian Museum of Nature, the Canterbury Museum, the Carnegie Museum of Natural History, CSIRO Sustainable Ecosystems, Australian National Wildlife Collection, the Department of Ornithology of the American Museum of Natural History, the Field Museum of Natural History, the Florida Museum of Natural History, the McGill University Redpath Museum, le Muséum National d’Histoire Naturelle, the Museum of New Zealand Te Papa Tongarewa, the Museum of Vertebrate Zoology, the University of California Berkeley, Museum Victoria, the Natural History Museum of Los Angeles County, the Ornithology Department of the Museum of Comparative Zoology of Harvard University, the Queen Victoria Museum and Art Gallery, the Queensland Museum, the Royal Alberta Museum, the Royal British Columbia Museum, the Royal Ontario Museum, the Sam Noble Oklahoma Museum of Natural History, the San Diego Natural History Museum, the Smithsonian Institution, the South Australian Museum, the University of Alaska Museum, the University of Kansas Natural History Museum, the University of Michigan Museum of Zoology, the University of Washington Burke Museum, the Western Australian Museum, the Yale University Peabody Museum and the Zoology Museum of the University of Copenhagen. We also thank Raoul Mulder and Devi Stuart-Fox for comments on earlier versions of this manuscript.


References

Afton, A. D. (1985). Forced copulation as a reproductive strategy of male lesser scaup: a field test of some predictions. Behaviour 92, 146–167.
Crossref | GoogleScholarGoogle Scholar | Andersson M. (1994). ‘Sexual Selection.’ (Princeton University Press: Princeton, NJ.)

Arnold, A. P. , Bottjer, S. W. , Brenowitz, E. A. , Nordeen, E. J. , and Nordeen, K. W. (1986). Sexual dimorphisms in the neural vocal control-system in song birds – ontogeny and phylogeny. Brain, Behavior and Evolution 28, 22–31.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Bellrose F. C. (1976). ‘Ducks, Geese and Swans of North America.’ (Stackpole Books: Harrisburg, PA.)

Bennett, P. M. , and Harvey, P. H. (1985). Relative brain size and ecology in birds. Journal of Zoology 207, 151–169.
Bordage D. , and Savard J. L. (1995). Black scoter (Melanitta nigra). In ‘The Birds of North America, No. 177’. (Eds A. Poole and F. Gill.) (The Academy of Natural Sciences: Philadelphia & The American Ornithologists’ Union: Washington, DC.)

Bowler J. (2005). Breeding strategies and biology. In ‘Ducks, Geese and Swans’. (Ed. J. Kear.) pp. 68–111. (Oxford University Press: New York.)

Braithwaite L. W. , and Norman F. I. (1974). The 1972 open season on waterfowl in south-eastern Australia. CSIRO Division of Wildlife Research Technical Paper No. 29.

Braithwaite L. W. , and Norman F. I. (1976). The 1973 and 1974 open seasons on waterfowl in south-eastern Australia. CSIRO Division of Wildlife Research Technical Memorandum No. 11.

Brennan, P. L. R. , Prum, R. O. , McCracken, K. G. , Sorenson, M. D. , Wilson, R. E. , and Birkhead, T. R. (2007). Coevolution of male and female genital morphology in waterfowl. PLoS ONE 2(5), e418.
Crossref | GoogleScholarGoogle Scholar | PubMed | Brewer G. L. (2005). Ringed teal Callonetta leucophrys. In ‘Ducks, Geese and Swans’. (Ed. J. Kear.) pp. 482–484. (Oxford University Press: New York.)

Brewer G. L. , and Port J. (2005). South American teal Anas flavirostris. In ‘Ducks, Geese and Swans’. (Ed. J. Kear.) pp. 613–616. (Oxford University Press: New York.)

Briggs S. V. (1990). Waterbirds. In ‘The Murray’. (Eds N. Mackay and D. Eastburn.) pp. 336–344. (Murray Darling Bassin Commission: Canberra.)

Byrne R. W. , and Whiten A. (1997). Machiavellian intelligence. In ‘Machiavellian Intelligence II: Extensions and Evaluations’. (Eds A. Whiten and R. W. Byrne.) pp. 1–23. (Cambridge University Press: Cambridge.)

Calhim, S. , and Birkhead, T. R. (2007). Testes size in birds: quality versus quantity – assumptions, errors, and estimates. Behavioral Ecology 18, 271–275.
Crossref | GoogleScholarGoogle Scholar | Cramp S. , and Simmons K. E. L. (1977). ‘Handbook of the Birds of Europe, the Middle East and North Africa. Volume 1: Ostrich to Ducks.’ (Oxford University Press: Oxford.)

Day, L. B. , Westcott, D. A. , and Olster, D. H. (2005). Evolution of bower complexity and cerebellum size in bowerbirds. Brain, Behavior and Evolution 66, 62–72.
Crossref | GoogleScholarGoogle Scholar | PubMed | Eadie J. M. , Mallory M. L. , and Lumsden H. G. (1995). Common goldeneye (Bucephala clangula). In ‘The Birds of North America Online’. (Ed. A. Poole.) (Cornell Laboratory of Ornithology: Ithaca, NY.)

Eadie J. M. , Savard J.-P. L. , and Mallory M. L. (2000). Barrow’s goldeneye (Bucephala islandica). In ‘The Birds of North America. No. 548’. (Eds A. Poole and F. Gill.) (The Birds of North America, Inc.: Philadelphia, PA.)

Ely, C. R. (1989). Extra-pair copulation in the greater white-fronted goose. The Condor 91, 990–991.
Crossref | GoogleScholarGoogle Scholar | Frith H. J. (1967). ‘Waterfowl in Australia.’ (Angus and Robertson Ltd: Sydney.)

Frith, H. J. , and Davis, S. J. J. F. (1961). Ecology of the magpie goose, Anseranas semipalmata Latham (Anatidae). CSIRO Wildlife Research 6, 91–141.
Fullagar P. (2005). Blue-billed duck Oxyura australis. In ‘Ducks, Geese and Swans’. (Ed. J. Kear.) pp. 358–361. (Oxford University Press: New York.)

Fullagar P. , Davey C. , Shepherd P. , and Peters C. (2005). Freckled duck Stictonetta naevosa. In ‘Ducks, Geese and Swans’. (Ed. J. Kear.) pp. 339–343. (Oxford University Press: New York.)

Gamble K. E. (1966). Breeding biology and food habits of the musk duck (Biziura lobata). M.Sc. Thesis, University of Wisconsin, Madison, WI.

Gammonley J. H. (1996). Cinnamon teal (Anas cyanoptera). In ‘The Birds of North America. No. 209’. (Eds A. Poole and F. Gill.) (The Academy of Natural Sciences: Philadelphia & The American Ornithologists’ Union: Washington, DC.)

Garamszegi, L. Z. , Eens, M. , Erritzoe, J. , and Møller, A. P. (2005). Sperm competition and sexually size dimorphic brains in birds. Proceedings of the Royal Society of London. Series B. Biological Sciences 272, 159–166.
Crossref | GoogleScholarGoogle Scholar | Goudie R. I. , Robertson G. J. , and Reed A. D. (2000). Common eider (Somateria mollissima). In ‘The Birds of North America. No. 546’. (Eds A. Poole and F. Gill.) (The Birds of North America, Inc.: Philadelphia, PA.)

Guay, P. J. , and Iwaniuk, A. N. (2008). Captive breeding reduces brain size in waterfowl (Anseriformes). The Condor 110, 276–284.
Crossref | GoogleScholarGoogle Scholar | Harvey P. A. (1988). Allometric analysis and brain size. In ‘Intelligence and Evolutionary Biology’. (Eds H. J. Jerison and I. Jerison.) pp. 199–210. (Springer-Verlag: Berlin.)

Healy, S. D. , and Rowe, C. (2007). A critique of comparative studies of brain size. Proceedings of the Royal Society of London. Series B. Biological Sciences 274, 453–464.
Crossref | GoogleScholarGoogle Scholar | Hepp G. R. , and Bellrose F. C. (1995). Wood duck (Aix sponsa). In ‘The Birds of North America. No. 169’. (The Academy of Natural Sciences: Philadelphia & The American Ornithologists’ Union: Washington, DC.)

Höhn, E. O. (1947). Sexual behaviour and seasonal changes in the gonads and adrenals of the Mallard. Proceeding of the Zoological Society of London 117, 281–304.
Johnsgard P. A. , and Carbonell M. (1996). ‘Ruddy Ducks and Other Stifftails: Their Behavior and Biology.’ (University of Oklahoma Press: Norman, OK.)

Johnson, K. P. , and Sorenson, M. D. (1999). Phylogeny and biogeography of dabbling ducks (genus: Anas): a comparison of molecular and morphological evidence. The Auk 116, 792–805.
Kear J. (1972). Reproduction and family life. In ‘The Swans’. (Eds P. Scott and W. Trust.) pp. 79–124. (Houghton Mifflin: Boston, MA.)

Kear J. (2005). ‘Ducks, Geese and Swans.’ (Oxford University Press: New York.)

Lavery H. J. (1964). An investigation of the biology and ecology of waterfowl (Anatidae: Anseriformes) in north Queensland. M.Sc. Thesis, University of Queensland, Brisbane.

Livezey, B. C. , and Humphrey, P. S. (1985). Territoriality and interspecific aggression in steamer-ducks. The Condor 87, 154–157.
Crossref | GoogleScholarGoogle Scholar | Longcore J. R. , McAuley D. G. , Hepp G. R. , and Rhymer J. M. (2000). American black duck (Anas rubripes). In ‘The Birds of North America. No. 481’. (Eds A. Poole and F. Gill.) (The Birds of North America, Inc.: Philadelphia, PA.)

Madden, J. (2001). Sex, bowers and brains. Proceedings of the Royal Society of London. Series B. Biological Sciences 268, 833–838.
Crossref | GoogleScholarGoogle Scholar | CAS | Madge S. , and Burn H. (1989). ‘Wildfowl, an Identification Guide to the Ducks, Geese and Swans of the World.’ (Christopher Helm: Bronley, UK.)

Mallory M. , and Metz K. (1999). Common merganser (Mergus merganser). In ‘The Birds of North America. No. 442’. (Eds A. Poole and F. Gill.) (The Birds of North America: Philadelphia, PA.)

Marchant S. , and Higgins P. J. (1990). ‘Handbook of Australian, New Zealand, and Antarctic Birds. Vol. 1B. Pelican to Ducks.’ (Oxford University Press: Oxford.)

Martins E. P. (2004). ‘COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Available at http://compare.bio.indiana.edu/ [Verified 2 February 2009].

Martins, E. P. , and Hansen, T. F. (1997). Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. American Naturalist 149, 646–667.
Crossref | GoogleScholarGoogle Scholar | McCarthy E. M. (2006). ‘Handbook of Avian Hybrids of the World.’ (Oxford University Press: Oxford.)

McCracken K. G. (2005). Musk duck Biziura lobata. In ‘Ducks, Geese and Swans’. (Ed. J. Kear.) pp. 213–217. (Oxford University Press: New York.)

McKinney F. (2005). Versicolor teal Anas versicolor. In ‘Ducks, Geese and Swans’. (Ed. J. Kear.) pp. 616–619. (Oxford University Press: New York.)

McKinney, F. , and Evarts, S. (1997). Sexual coercion in waterfowl and other birds. Ornithological Monographs 49, 163–195.
Miller G. (2000). ‘The Mating Mind.’ (William Heinemann: London.)

Mineau, P. , and Cooke, F. (1979). Rape in the lesser snow goose. Behaviour 70, 280–291.
Crossref | GoogleScholarGoogle Scholar | Moorman T. E. , and Gray P. N. (1994). Mottled duck (Anas fulvigula). In ‘The Birds of North America. No. 81’. (Eds A. Poole and F. Gill.) (The Academy of Natural Sciences, Philadelphia, PA & The American Ornithologists’ Union, Washington, DC.)

Mori, J. G. , and George, J. C. (1978). Seasonal histological changes in the gonads, thyroid and adrenal of the Canada goose (Branta canadensis interior). Acta Anatomica 101, 304–324.
CAS | PubMed | Ryder J. P. , and Alisauskas R. T. (1995). Ross’s goose (Chen rossii). In ‘The Birds of North America. No. 162’. (Eds A. Poole and F. Gill.) (The Academy of Natural Sciences, Philadelphia, PA & The American Ornithologists’ Union, Washington, DC.)

Savard, J.-P. L. (1985). Evidence of long-term pair bonds in Barrow’s goldeneye (Bucephala islandica). The Auk 102, 389–391.
Suydam R. S. (2000). King eider (Somateria spectabilis). In ‘The Birds of North America. No. 491’. (Eds A. Poole and F. Gill.) (The Birds of North America, Inc.: Philadelphia, PA.)

Titman R. D. (1999). Red-breasted merganser (Mergus serrator). In ‘The Birds of North America. No. 443’. (Eds A. Poole and F. Gill.) (The Birds of North America: Philadelphia, PA.)

Todd F. S. (1979). ‘Waterfowl: Ducks, Geese and Swans of the World.’ (Sea World Press: San Diego, CA.)

Ugelvik M. (1986). ‘Spacing Pattern and Social Behaviour in Breeding Wigeon Anas penelope.’ (University of Bergen: Norway.)

Veselovsky, Z. (1970). Zur Ethologie der Hühnergans (Cereopsis novaehollandiae Lath.). Zeitschrift für Tierpsychologie 27, 915–945.
Young G. (2005). African comb duck Sarkidiornis melanotos. In ‘Ducks, Geese and Swans’. (Ed. J. Kear.) pp. 391–393. (Oxford University Press: New York.)





Appendix 1.  Raw data used for the analysis
Sample size (nM and nF) and brain volume (mL) for males and females (BV M and BV F), body mass (g) for males and females (BM M and BM F), testicular mass (g) from fresh mass and linear measurement datasets (TMFM and TMLM), mating strategy (MS: 1, monogamous, no FEPC or no EPP; 2, infrequent FEPC; 3, frequent FEPC; and 4, polygynous or promiscuous), phallus length (cm; Phallus) and length of pair bond (PB: 0, no pair bond; 1, seasonal pair bond; and 2, multi-year pair bond) are listed. Sources for both TM and MS are listed at the foot of the table
Click to zoom