Seals have adapted their social systems and lactation strategies to marine environments that include open and ice-covered oceans, high and low productivity, extremes in seasonality, and ocean- and terrestrial-type predators. Different explanations for the variation in pinniped lactation systems have been proposed but tests of alternative hypotheses have not sufficiently accounted for phylogeny and body size. After controlling for this variation, I predicted that environment, mating habitat, and predation would yield a fuller explanation. Lactation traits, duration, pup growth rate, and fat content were significantly influenced by both body size and phylogeny, which together explained 20–69% of the variation. After controlling for this variation, initial results did not support the environment hypothesis, as no differences in lactation traits were found between species living in polar (≥60°N) versus equatorial (<60°N) environments. In contrast, seals that nurse in areas of Arctic sea ice contending with ice-hunting predators, such as polar bears, had relatively short lactation compared to species living in the Antarctic and more equatorial regions. Also, the availability of predator-free islands for terrestrial mating and parturition was related to a harem mating system, increased sexual size dimorphism (SSD), and slow juvenile growth rates, less fat in milk, and longer lactation. Using structural equation modeling, latitude and size of harems provided independent explanations for all three lactation traits. Thus, use of islands in ice-free waters, predation in Arctic ice-covered waters, and more milk fat in high-latitude seals together provided adequate explanations for the evolution of lactation diversity among pinnipeds.
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LITERATURE CITED
Anderson, D. R., Burnham, K. P., and Thompson, W. L. (2000). Null hypothesis testing: Problems, prevalence, and an alternative. J. Wildl. Manage. 64: 912–923.
Atkinson, S. (1997). Reproductive biology of seals. Rev. Reproduction 2: 175–194.
Bartholomew, G. A. (1970). A model for the evolution of pinniped polygyny. Evolution 24: 546–559.
Bentler, P. M. (1983). Some contributions to efficient statistics in structural models: Specification and estimation of moment structures. Psychometrika 48: 493–517.
Bininda-Emonds, O. R. P. (2004a). The evolution of supertrees. Trends Ecol. Evol. 19: 315–322.
Bininda-Emonds, O. R. P. (2004b). Trees versus characters and the supertree/supermatrix “paradox.” Syst. Biol. 53: 356–359.
Bininda-Emonds, O. R. P., Gittleman, J. L., and Purvis, A. (1999). Building large trees by combining phylogenetic information: A complete phylogeny of the extant Carnivora (Mammalia). Biol. Rev. 74: 143–175.
Bininda-Emonds, O. R. P., Gittleman, J. L., and Steel, M. A. (2002). The (super)tree of life: Procedures, problems, and prospects. Annu. Rev. Ecol. Syst. 33: 265–289.
Blomberg, S. P., Garland, T., Jr., and Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution 57: 717–745.
Boness, D. J. (1991). Determinants of mating systems in the Otariidae (Pinnipedia). In: The Behaviour of Pinnipeds, D. Renouf, ed., pp. 1–44, Chapman and Hall, London, UK.
Boness, D. J., and Bowen, W. D. (1996). The evolution of maternal care in pinnipeds. BioScience 46: 645–654.
Bonner, W. N. (1984). Lactation strategies in pinnipeds: Problems for a marine mammalian group. Symp. Zool. Soc. Lond. 51: 253–272.
Boyd, I. L. (1991). Environmental and physiological factors controlling the reproductive cycles of pinnipeds. Can. J. Zool. 69: 1135–1148.
Boyd, I. L. (1998). Time and energy constraints in pinniped lactation. Am. Nat. 152: 717–728.
Bowen, W. D., Oftedal, O. T., and Boness, D. J. (1985). Birth to weaning in 4 days: Remarkable growth in the hooded seal, Cystophora cristata. Can. J. Zool. 63: 2841–2846.
Bowen, W. D., Iverson, S. J., Boness, D. J., and Oftedal, O. T. (2001). Foraging effort, food intake and lactation performance depend on maternal mass in a small phocid seal. Funct. Ecol. 15: 325–334.
Bozdogan, H. (1987). Model selection and Akaike's Information Criterion (AIC): The general theory and its analytical extensions. Psychometrika 52: 345–370.
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M., and West, G. B. (2004). Toward a metabolic theory of ecology. Ecology 85: 1771–1789.
Burnham, K. P., and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, Springer, New York.
Calder, W. A., III (1984). Size, Function and Life History, Harvard University Press, Cambridge, UK.
Caudron, A. K. (1997). Pinnipeds social systems: A review. Mammalia 61: 153–160.
Costa, D. P. (1991). Reproductive and foraging energetics of high latitude penguins, albatrosses and pinnipeds: Implications for life history patterns. Am. Zool. 31: 111–130.
Davis, C. S., Delisle, I., Stirling, I., Siniff, D. B., and Strobeck, C. (2004). A phylogeny of the extant Phocidae inferred from complete mitochondrial DNA coding regions. Mol. Phylogenet. Evol. 33: 363–377.
Deecke, V. B., Slater, P. J. B., and Ford, J. K. B. (2002). Selective habituation shapes acoustic predator recognition in harbour seals. Nature 420: 171–173.
Delisle, I., and Strobeck, C. (2005). A phylogeny of the Caniformia (order Carnivora) based on 12 complete protein-coding mitochondrial genes. Mol. Phylogenet. Evol. 37: 192–201.
Emlen, S. T., and Oring, L. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197: 215–233.
Estrada, J. A., Rice, A. N., Lutcavage, M. E., and Skomal, G. B. (2004). Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. J. Mar. Biol. Ass. U.K. 83: 1347–1350.
Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125: 1–15.
Ferguson, S. H. (2002). Using survivorship curves to estimate age of first reproduction in moose Alces alces. Wildl. Biol. 8: 129–136.
Ferguson, S. H., and Larivière, S. (2004). Are long penis bones an adaptation to high latitude snowy environments? Oikos 105: 255–267.
Ferguson, S. H., Virgl, J. A., and Larivière, S. (1996). Evolution of delayed implantation and associated grade shifts in life history traits of North American carnivores. Ecoscience 3: 7–17.
Furgal, C. M., Innes, S., and Kovacs, K. M. (1996). Characteristics of ringed seal Phoca hispida, subnivean structures and breeding habitat and their effects on predation. Can. J. Zool. 74: 855–874.
Furgal, C. M., Innes, S., and Kovacs, K. M. (2002). Inuit spring hunting techniques and local knowledge of the ringed seal in Arctic Bay (Ilkpiarjuk), Nunavut. Pol. Res. 21: 1–16.
Garland, T., Jr., Dickerman, A. W., Janis, C. M., and Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Syst. Biol. 42: 265–292.
Garland, T., Jr., Midford, P. E., and Ives, A. R. (1999). An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am. Zool. 39: 374–488.
Garland, T., Jr., Midford, P. E., Jones, J. A., Dickerman, A. W., and Diaz-Uriarte, R. (2001). PDAP: Phenotypic Diversity Analysis Programs, Version 6.0, University of California, California.
Gatesy, J., and Springer, M. (2005). A critique of matrix representation with parsimony supertrees. In: Phylogenetic Supertrees: Combining Information to Reveal the Tree of Life, O. R. P. Bininda-Emonds, ed., pp. 369–388, Computational Biology Series, Kluwer Academic, Dordrecht, The Netherlands.
Gatesy, J., Matthee, C., DeSalle, R., and Hayashi, C. (2002). Resolution of a supertree/supermatrix paradox. Syst. Biol. 51: 652–664.
Gatesy, J., Baker, R. H., and Hayashi, C. (2004). Inconsistencies in arguments for the supertree approach: Supermatrices versus supertrees of Crocodylia. Syst. Biol. 53: 342–355.
Gittleman, J. L., and Oftedal, O. T. (1987). Comparative growth and lactation energetics in carnivores. Symp. Zool. Soc. Lond. 57: 41–77.
Hairston, N. G., Jr., and Hairston, N. G., Sr. (1993). Cause–effect relationships in energy flow, trophic structure, and interspecific interactions. Am. Nat. 142: 379–411.
Harvey, P. H., and Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology, Oxford University Press, Oxford, UK.
Heise, K., Barrett-Lennard, L. G., Saulitis, E., Matkin, C., and Bain, D. (2003). Examining the evidence for killer whale predation on Steller sea lions in British Columbia and Alaska. Aquatic Mamm. 29: 325–334.
Jenness, R., and Sloan, R. E. (1970). The composition of milks of various species: A review. Dairy Sci. Abst. 32: 599–612.
Kangas, A. T., Evans, A. R., Thesleff, I., and Jernvall, J. (2004). Nonindependence of mammalian dental characters. Nature 432: 211–214.
Kleiber, M. (1932). Body size and metabolism. Hilgardia 6: 315–332.
Kovacs, K. M., and Lavigne, D. M. (1986). Maternal investment and neonatal growth in Phocid seals. J. Anim. Ecol. 55: 1035–1051.
Kovacs, K. M., and Lavigne, D. M. (1992). Maternal investment in otariid seals and walruses. Can. J. Zool. 70: 1953–1964.
Lindenfors, P., Tullberg, B. S., and Biuw, M. (2002). Phylogenetic analysis of sexual selection and sexual size dimorphism. Behav. Ecol. Sociobiol. 52: 188–193.
Lima, S. L. (2002). Putting predators back into behavioural predator–prey interactions. Trends Ecol. Evol. 17: 70–75.
Lydersen, C., and Hammill, M. O. (1993). Activity, milk intake and energy consumption in free-living ringed seal (Phoca hispida) pups. J. Comp. Phys. B Biochem. Syst. Environ. Phys. 163: 433–438.
McIntire, E. J. B. (2004). Understanding natural disturbance boundary formation using spatial data and path analysis. Ecology 85: 1933–1943.
Millar, J. S. (1977). Adaptive features of mammalian reproduction. Evolution 31: 370–386.
Oftedal, O. T., Boness, D. J., and Tedman, R. A. (1987). The behaviour, physiology, and anatomy of lactation in the pinnipedia. Current Mamm. 1: 175–245.
Partridge, L., and Harvey, P. H. (1988). The ecological context of life history evolution. Science 241: 1449–1455.
Petraitis, P. S., Dunham, A. E., and Niewiarowski, P. H. (1996). Inferring multiple causality: The limitations of path analysis. Funct. Ecol. 10: 421–431.
Purvis, A. (1995). A composite estimate of primate phylogeny. Philos. Trans. R. Soc. Lond. B 348: 405–421.
Pond, C. M. (1977). The significance of lactation in the evolution of mammals. Evolution 31: 177–199.
Quinn, J. F., and Dunham, A. E. (1983). On hypothesis testing in ecology and evolution. Am. Nat. 122: 602–617.
Ralls, K. (1977). Sexual dimorphism in mammals: Avian models and unanswered questions. Am. Nat. 981: 917–938.
SAS Institute (1999). SAS/STAT ® Users Guide, Version 6, SAS Institute, Cary, USA.
Schulz, T. M., and Bowen, W. D. (2004). Pinniped lactation strategies: Evaluation of data on maternal and offspring life history traits. Mar. Mamm. Sci. 20: 86–114.
Schulz, T. M., and Bowen, W. D. (2005). The evolution of lactation strategies in pinnipeds: A phylogenetic analysis. Ecol. Monogr. 75: 159–177.
Schwarz, G. (1978). Estimating the dimension of a model. Ann. Stat. 6: 461–464.
Shipley, B. (2000). Cause and Correlation in Biology: A User’s Guide to Path Analysis, Structural Equations and Causal Inference, Cambridge University Press, Cambridge, U.K.
Sih, A. (1985). Evolution, predator avoidance and unsuccessful predation. Am. Nat. 125: 153–157.
Smith, T. G. (1976). Predation of ringed seal pups (Phoca hispida) by the Arctic fox (Alopex lagopus). Can. J. Zool. 54: 1610–1616.
Sokal, R. R., and Rohlf, F. J. (1995). Biometry, W. H. Freeman, San Francisco, USA.
Springer, M. S., and de Jong, W. W. (2001). Which mammalian supertree to bark up? Science 291: 1710–1711.
Stewart, B. E., Innes, S., and Stewart, R. E. A. (1998). Mandibular dental ontogeny of ringed seals (Phoca hispida). Mar. Mamm. Sci. 14: 221–231.
Stirling, I. (1975). Factors affecting the evolution of social behaviour in the pinnipedian. Rapports et Proces-Verbaux des Reunions Cousel International Pour L’explora de la Mer 169: 205–212.
Stirling, I. (1977). Adaptations of Weddell and ringed seals to exploit the polar fast ice habitat in the absence and presence of surface predators. In: Adaptations Within Antarctic Ecosystems. Proceedings 3rd SCAR Symposium on Antarctic Biology, Washington, DC, August 26–30, 1974, G. A. Llano, ed., pp. 741–748, Gulf Publishing Company, Houston, USA.
Stirling, I. (1983). The evolution of mating systems in pinnipeds. In: Advances in the Study of Mammalian Behaviour, J. F. Eisenberg, ed., pp. 489–527, Am. Soc. Mammal., Special Publication No. 7.
Thornthwaite, C. W., and Mather, J. R. (1957). Instructions and tables for computing potential evapotranspiration and the water balance. Drexel Institute of Technology, Laboratory of Climatology. Publ. Climat. 10: 181–311.
Trivers, R. L. (1972). Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, B. Campbell, ed., pp. 136–179, Aldine Press, Chicago, USA.
Van Parijs, S. M. (2003). Aquatic mating in pinnipeds: A review. Aquatic Mamm. 29: 214–226.
Wilmott, C. J., Rowe, C. M., and Mintz, Y. (1985). Climatology of the terrestrial seasonal water cycle. J. Climatol. 5: 589–606.
ACKNOWLEDGMENTS
NSERC Discovery Grant (250465-03) and ArcticNet supported this research. Earlier drafts of this paper were greatly improved by discussions and critical reviews by the editor, M. S. Springer, an anonymous reviewer, W. D. Bowen, and R. E. A. Stewart.
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Ferguson, S.H. The Influences of Environment, Mating Habitat, and Predation on Evolution of Pinniped Lactation Strategies. J Mammal Evol 13, 63–82 (2006). https://doi.org/10.1007/s10914-005-9003-1
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DOI: https://doi.org/10.1007/s10914-005-9003-1