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  • Cited by 2
  • Print publication year: 2008
  • Online publication date: August 2009

3 - Phylogenetic analysis of alternative reproductive tactics: problems and possibilities

Summary

CHAPTER SUMMARY

We present an outline of the potential that a phylogenetic approach may bring to the study of alternative reproductive tactics (ARTs) and discuss some of the difficulties and methodological problems that must be addressed if we are to apply the phylogenetic method successfully. We illustrate the principles presented by applying them to three selected examples. Specifically, based on fish studies, ARTs are, at least in some fish groups, evolutionarily unstable and rarely become incorporated as a fixed trait of a lineage at a rank as high as a family. Despite this instability, it is common for a given lineage to give rise recurrently to very similar forms of ARTs. Our results illustrate the wide spectrum of potential studies that can be enriched by a phylogenetic perspective.

BACKGROUND

The role of phylogenetic studies in the behavioral sciences

When Tinbergen (1963) formulated his famous four levels of explanation in ethology – causation, development, evolution, and function – the study of patterns in the evolution of behavior was explicitly made one of the central aims of the study of animal behavior. Each behavior pattern has an evolutionary history, and often it is possible to trace its origins, identifying the behavior that existed prior to the emergence of the new patterns. The pioneering work of Konrad Lorenz, who used behavior patterns to help to clarify the taxonomy of ducks, illustrates the use of behavioral phylogenies in an outstanding way (Lorenz 1941).

References
Almada, V. C. and Santos, R. S. 1995. Parental care in the rocky intertidal: a case study of adaptation and exaptation in Mediterranean and Atlantic blennies. Reviews in Fish Biology and Fisheries 5, 23–37.
Almada, F., Almada, V. C., Domingues, V., Brito, A., and Santos, R. S. 2005a. Molecular validation of the specific status of Parablennius sanguinolentus and Parablennius parvicornis (Pisces: Blenniidae). Scientia Marina 69, 519–523.
Almada, F., Almada, V., Guillemaud, T., and Wirtz, P. 2005b. Phylogenetic relationships of the north-eastern Atlantic and Mediterranean blenniids. Biological Journal of the Linnean Society 86, 283–295.
Almada, V., Almada, F., Henriques, M., Santos, R. S., and Brito, A. 2002. On the phylogenetic affinities of Centrolabrus trutta and Centrolabrus caeruleus (Perciformes: Labridae) to the genus Symphodus: molecular, meristic and behavioural evidences. Arquipélago: Life and Marine Sciences 19A, 85–92.
Blanchefield, P. J., Ridgway, M. S., and Wilson, C. C. 2003. Breeding success of male brook trout (Salvelinus fontinalis) in the wild. Molecular Ecology 12, 2417–2428.
Brooks, D. R. and McLennan, D. A. 1991. Phylogeny, Ecology, and Behavior: A Research Program in Comparative Biology. Chicago, IL: University of Chicago Press.
Crespi, B. J. and Fulton, M. J. 2004. Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny. Molecular Phylogenetics and Evolution 31, 658–679.
DeWoody, J. A., Fletcher, D. E, Wilkins, S. D., Nelson, W. S., and Avise, J. C. 1998. Molecular genetic dissection of spawning, parentage, and reproductive tactics in a population of redbreast sunfish Lepomis auritus. Evolution 52, 1802–1810.
DeWoody, J. A., Fletcher, D. E., Mackiewicz, M., Wilkins, S. D., and Avise, J. C. 2000. The genetic mating system of spotted sunfish (Lepomis punctatus): mate numbers and the influence of male reproductive parasites. Molecular Ecology 9, 2119–2128.
Froese, R. and Pauly, D. (eds.) 2005. FishBase. Available online at www.fishbase.org, version (05/2005).
Garant, D., Dodson, J. J., and Bernatchez, L. 2003. Differential reproductive success and heritability of alternative reproductive tactics in wild Atlantic salmon (Salmo salar L.). Evolution 57, 1133–1141.
Garcia-Vazquez, E., Moran, P., Martinez, J. L., et al. 2001. Alternative mating strategies in Atlantic salmon and brown trout. Journal of Heredity 92, 146–149.
Gonçalves, D., Fagundes, T., and Oliveira, R. 2003. Reproductive behaviour of sneaker males of the peacock blenny. Journal of Fish Biology 63, 528–532.
Gonçalves, E. J., Almada, V. C., Oliveira, R. F., and Santos, A. J. 1996. Female mimicry as a mating tactic in males of the blenniid fish Salaria pavo. Journal of the Marine Biological Association of the United Kingdom 76, 529–538.
Goodwin, N. B., Balshine-Earn, S., and Reynolds, J. D. 1998. Evolutionary transitions in parental care in cichlid fish. Proceedings of the Royal Society of London B 265, 2265–2272.
Gould, S. J. and Vrba, E. S. 1982. Exaptation: a missing term in the science of form. Paleobiology 8, 4–15.
Gross, M. R. 1982. Sneakers, satellites and parentals: polymorphic mating strategies in North American sunfishes. Zeitschrift für Tierpsychologie 60, 1–26.
Gross, M. R. 1984. Sunfish, salmon, and the evolution of alternative reproductive strategies and tactics in fishes. In Wootton, R. and Potts, G. (eds.) Fish Reproduction: Strategies and Tactics, pp. 55–75. London: Academic Press.
Gross, M. R. and Charnov, E. L. 1980. Alternative male life histories in bluegill sunfish. Proceedings of the National Academy of Sciences of the United States of America 77, 6937–6940.
Haase, M. 2005. Rapid and convergent evolution of parental care in hydrobiid gastropods from New Zealand. Journal of Evolutionary Biology 18, 1076–1086.
Hall, B. G. 2004. Phylogenetic Trees Made Easy, 2nd edn. Sunderland, MA: Sinauer Associates.
Hanel, R., Westneat, M., and Sturmbauer, C. 2002. Phylogenetic relationships, evolution of broodcare behaviour, and geographic speciation in the wrasse tribe Labrini. Journal of Molecular Evolution 55, 776–789.
Harvey, P. H. and Pagel, M. D. 1991. The Comparative Method in Evolutionary Biology. Oxford, UK: Oxford University Press.
Harvey, P. H., Leigh Brown, A. J., Maynard Smith, J., and Nee, S. (eds.) 1996. New Uses for New Phylogenies. Oxford, UK: Oxford University Press.
Hennig, W. 1965. Phylogenetic systematics. Annual Review of Entomology 10, 97–116.
Hennig, W. 1966. Phylogenetic Systematics. Urbana, IL: University of Illinois Press.
Hino, T., Maekawa, K., and Reynolds, J. B. 1990. Alternative male mating behaviours in landlocked Dolly Varden (Salvelinus malma) in south-central Alaska. Journal of Ethology 8, 13–20.
Koblmüller, S., Salzburger, W., and Sturmbauer, C. 2004. Evolutionary relationships in the sand-dwelling cichlid lineage of Lake Tanganyika suggest multiple colonization of rocky habitats and convergent origin of biparental mouthbrooding. Journal of Molecular Evolution 58, 79–96.
Koseki, Y. and Maekawa, K. 2002. Differential energy allocation of alternative male tactics in masu salmon (Oncorhynchus masou). Canadian Journal of Fisheries and Aquatic Sciences 59, 1717–1723.
Lorenz, K. 1941. Vergleichende Bewegungsstudien an Anatinen. Journal für Ornithologie (Ergänzungsband 3) 89, 194–294.
Mackiewicz, M., Fletcher, D. E., Wilkins, S. D., DeWoody, J. A., and Avise, J. C. 2002. A genetic assessment of parentage in a natural population of dollar sunfish (Lepomis marginatus) based on microsatellite markers. Molecular Ecology 11, 1877–1883.
Maddison, W. P. and Maddison, D. R. 2005. Mesquite: A Modular System for Evolutionary Analysis, version 1.06. Available online at http://mesquiteproject.org.
Martinez, J. L., Moran, P., Perez, J., et al. 2000. Multiple paternity increases effective size of southern Atlantic salmon populations. Molecular Ecology 9, 293–298.
Martins, E. P. (ed.) 1996. Phylogenies and the Comparative Method in Animal Behavior. Oxford, UK: Oxford University Press.
McPhail, J. D. and Baxter, J. S. 1996. A Review of Bull Trout (Salvelinus confluentus) Life-History and Habitat Use in Relation to Compensation and Improvement Opportunities, Fisheries Management Report No. 104. Vancouver, BC.
Moran, P. and Garcia-Vazquez, E. 1998. Multiple paternity in Atlantic salmon: a way to maintain genetic variability in relicted populations. Journal of Heredity 89, 551–553.
Neat, F. C., Lengkeek, W., Westerbeek, E. P., Laarhoven, B., and Videler, J. J. 2003a. Behavioural and morphological differences between lake and river populations of Salaria fluviatilis. Journal of Fish Biology 63, 374–387.
Neat, F. C., Locatello, L., and Rasotto, M. B. 2003b. Reproductive morphology in relation to alternative male reproductive tactics in Scartella cristata. Journal of Fish Biology 62, 1381–1391.
Neff, B. D. 2001. Genetic paternity analysis and breeding success in bluegill sunfish (Lepomis macrochirus). Journal of Heredity 92, 111–119.
Nelson, J. S. 2006. Fishes of the World, 4th edn.New York: John Wiley.
Oliveira, R. F., Almada, V. C., Forsgren, E., and Gonçalves, E. J. 1999. Temporal variation in male traits, nesting aggregations and mating success in the peacock blenny, Salaria pavo. Journal of Fish Biology 54, 499–512.
Oliveira, R. F., Almada, V. C., Gonçalves, E. J., Forsgreen, E., and Canário, A. V. M. 2001a. Androgen levels in males and social interactions in breeding males of the peacock blenny. Journal of Fish Biology 58, 897–908.
Oliveira, R. F., Canário, A. V. M., and Grober, M. S. 2001b. Male sexual polymorphism, alternative reproductive tactics and androgens in combtooth blennies (Pisces: Blenniidae). Hormones and Behavior 40, 266–275.
Page, R. D. M. and Holmes, E. C. 1998. Molecular Evolution: A Phylogenetic Approach. Oxford, UK: Blackwell Scientific.
Peach, M. B. and Rouse, G. W. 2004. Phylogenetic trends in the abundance and distribution of pit organs of elasmobranches. Acta Zoologica 85, 233–244.
Ruchon, F., Laugier, T., and Quignard, J. P. 1995. Alternative male reproductive strategies in the peacock blenny. Journal of Fish Biology 47, 826–840.
Santos, R. S. 1995. Anatomy and histology of secondary sexual characters, gonads and liver of the rock-pool blenny (Parablennius sanguinolentus parvicornis) of the Azores. Arquipélago: Life and Marine Sciences 13A, 21–38.
Santos, R. S., Hawkins, S. J., and Nash, R. D. M. 1996. Reproductive phenology of the Azorean rock-pool blenny (Parablennius sanguinolentus parvicornis), a fish with alternative mating tactics. Journal of Fish Biology 48, 842–858.
Taborsky, M. 1994. Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Advances in the Study of Behavior 23, 1–100.
Taborsky, M. 1998. Sperm competition in fish: “bourgeois” males and parasitic spawning. Trends in Ecology and Evolution 13, 222–227.
Taborsky, M. 1999. Conflict or cooperation: what determines optimal solutions to competition in fish reproduction? In Oliveira, R., Almada, V., and Gonçalves, E. (eds.) Behaviour and Conservation of Littoral Fishes, pp. 301–349. Lisbon: Instituto Superior de Psicologia Aplicada.
Taborsky, M. 2001. The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. Journal of Heredity 92, 100–110.
Tinbergen, N. 1963. On aims and methods of ethology. Zeitschrift für Tierpsychologie 20, 410–433.
Wiegmann, D. D., Baylis, J. R., and Hoff, M. H. 1997. Male fitness, body size and timing of reproduction in smallmouth bass, Micropterus dolomieui. Ecology 78, 111–128.
Willson, M. F. 1997. Variation in Salmonid Life Histories: Patterns and Perspectives, Research Paper No. 498. United States Department of Agriculture Forest Service, Pacific Northwest Research Station.
Wilson, A. B., Ahnesjö, I., Vincent, A. C. J., and Meyer, A. 2003. The dynamics of male brooding, mating patterns and sex roles in pipefishes and seahorses (Family Syngnathidae). Evolution 57, 1374–1386.