Abstract
Several hypotheses that involve either sexual selection (intra- and intersexual) or disruptive ecological selection (e.g., niche divergence, reproductive role division) or both have been advanced as adaptive explanations for the evolution and maintenance of sexual size dimorphism (SSD). However, ever since Darwin, the prevalent explanation in species with male-biased SSD has been intrasexual selection favoring larger size in males in the competition for mates. Here, I show that in the Galapagos Flightless cormorant (Phalacrocorax harrisi; Phalacrocoracidae), the sexes differ significantly in body mass and in all five external morphometric traits measured, with body mass being the most dimorphic trait followed by bill width and bill depth. Correlations between morphometric traits and between morphometric traits and body mass differed by trait and by sex. Comparative analyses including 16 other species within the family showed that the Flightless cormorant is the largest phalacrocoracid. Several factors are theoretically likely to favor the evolution of larger size and greater SSD in species where the male is larger than the female. However, sexual selection favoring larger size in males through competition for mates or by mate choice all seem unlikely explanations for SSD in the Flightless cormorant. Here, I argue that the main driving force for the evolution of the species’ larger size is disruptive ecological selection involving selection for larger body size in males as an adaptation for larger prey and genetic correlation between the sexes for body size explain the increased size and larger sexual dimorphism of the species. Comparative analyses also showed that the Flightless cormorant has a significantly greater sexual dimorphism in both body mass and bill depth, but dimorphism in bill length was similar to that of other Phalacrocoracidae. Thus, the Flightless cormorant is the most sexually dimorphic of the Phalacrocoracidae. The degree of sexual dimorphism in all traits correlated positively and strongly with mean body mass of each sex and with the mean of both sexes combined. However, the slope of reduced major axis (RMA) regressions of male traits as function of female traits, except for bill depth, did not depart significantly from geometric isometry (β = 1.0), showing that Phalacrocoracidae do not follow Rensch’s rule. Thus, among phalacrocoracids, variation in body size fully explains variation in the degree of interspecific variation in SSD and sexual dimorphism in other traits. This means that a remarkable SSD and sexual dimorphism in other traits in the Flightless cormorant relative to other phalacrocoracids can simply be attributable to the species’ largest size; thus, the magnification of sexual dimorphism, including SSD, is an effect of disruptive ecological selection favoring larger size in males and consequently a lower rate of increase in female size as a correlated response similar to that in other phalacrocoracids resulting from genetic correlation between the sexes for body size. I also suggest that the remarkable larger size (gigantism) and remarkable sexual dimorphism of the Flightless cormorant are both novel character states that have evolved in situ following colonization of the Galapagos Islands.
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References
Abouheif E, Fairbairn DJ (1997) A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am Nat 149:340–362
Alexander RD, Hoogland JL, Howard RD, Noonan KM, Sherman PW (1979) Sexual dimorphism and breeding systems in pinnipeds, ungulates, primates and humans. In: Chagnon NA, Irons W, Scituate MA (eds) Evolutionary biology and human social behavior: an anthropological perspective. Duxbury, pp 402–435
Anderson M (1994) Sexual selection. Princeton University Press, Princeton
Berry JF, Shine R (1980) Sexual dimorphism and sexual selection in turtles (order Testudines). Oecologia 44:185–191
Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 75:385–407
Bohonak AJ (2004) Software for reduced major axis regression, V.1.17. San Diego State University
Butler MA, Schoener TW, Losos JB (2000) The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards. Evolution 54:259–272
Calder WA (1984) Size, function, and life history. Cambridge, Harvard University Press
Cheverud JM, Dow MM, Leutenegger W (1985) The quantitative assessment of Phylogenetic constraints in comparative analyses: sexual dimorphism in body weight among primates. Evolution 39:1335–1351
Clutton-Brock TH, Harvey PH, Rudder B (1977) Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269:797–800
Cox RM, Skelly SL, John-Alder HB (2003) A comparative test of adaptive hypotheses for sexual size dimorphism in lizards. Evolution 57:1653–1669
Darwin C (1871) The descent of man and selection in relation to sex, 1st edn. John Murray, London
Downhower JF (1976) Darwin’s finches and the evolution of sexual dimorphism in body size. Nature 263:558–563
Emerson SB (1994) Testing pattern predictions of sexual selection. Am Nat 143:848–869
Fairbairn DJ (1997) Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Ann Rev Ecol Syst 28:659–687
Fairbairn DJ (2005) Allometry for sexual size dimorphism: testing two hypotheses for Rensch’s rule in the water strider Aquarius remigis. Am Nat 166:69–84
Fairbairn DJ, Preziosi RF (1994) Sexual selection and the evolution of allometry for sexual size dimorphism in the water strider, Aquariusremigis. Am Nat 144:101–108
Fairbairn DJ, Shine R (1993) Patterns of sexual size dimorphism in seabirds of the southern hemisphere. Oikos 68:139–145
Fairbairn DJ, Blanckenhorn WU, Szekely T (2007) Sex, size, and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford
Gaulin SJC, Sailer LD (1984) Sexual dimorphism in weight among the Primates: the relative impact of allometry and sexual selection. Int J Primatol 5:515–535
Gibbs HL, Grant PR (1987) Oscillating selection on Darwin’s finches. Nature 327:511–513
Grant PR (1968) Bill size, body size, and the ecological adaptations of bird species to competitive situations on islands. Syst Zool 17:319–333
Grant PR (1999) Ecology and evolution of Dartwin’s finches, 2nd edn. Princeton University Press, Princeton
Grant PR, Grant BR (2008) How and why species multiply: the radiation of Darwin’s finches. Princeton University Press, Princeton
Harris MP (1979) Population dynamics of the Flightless cormorant Nannopterum harrisi. Ibis 121:135–146
Hedrick AV, Temeles EJ (1989) The evolution of sexual dimorphism in animals: hypotheses and tests. Trends Ecol Evol 4:136–138
Herrel A, Spithoven L, Van Damme R, De Vree F (1999) Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analyses. Funct Ecol 13:289–297
Jehl JR Jr, Murray BG Jr (1986) The evolution of normal and reverse sexual size dimorphism in shorebirds and other birds. Curr Ornithol 3:1–86
Johnsgard PA (1993) Cormorants, darters, and pelicans of the world. Smithsonian Institution Press, Washington
Karubian J, Swaddle JP (2001) Selection on females can create ‘larger males’. Proc R Soc Lond B Biol Sci 268:725–728
Kennedy M, Gray RD, Spence HG (2000) The phylogenetic relationships of the shags and cormorants: can sequence data resolve a disagreement between behavior and morphology? Mol Phyl Evol 17:345–359
Kennedy M, Valle CA, Spencer HG (2009) The phylogenetic position of the Galápagos Cormorant. Mole Phylogenet Evol 53:94–98
LaBarbera M (1989) Analyzing body size as a factor in ecology and evolution. Annu Rev Ecol Syst 20:97–117
Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305
Lande R, Arnold SJ (1985) Evolution of mating preference and sexual dimorphism. J Theor Biol 117:651–664
Lederer RJ (1975) Bill size, food size, and jaw forces of insectivorous birds. Auk 92:385–387
Leutenegger W, Cheverud J (1982) Correlates of sexual dimorphism in primates: ecological and size variables. Int J Primatol 3:387–402
Leutenegger W (1978) Scaling of sexual dimorphism in body size and breeding system in primates. Nature 272:610–611
Livezey BC (1992) Flightlessness in the Galapagos Cormorant (Compsohalieus [Nannopterum] harrisi): heterochrony, giantisms and specialization. Zool J Linn Soc 105:155–224
Maynard SJ (1977) Parental investment: a prospective analysis. Anim Behav 25:1–9
Miles DB, Ricklefs RE (1984) The correlation between ecology and morphology in deciduous forest passerine birds. Ecology 65(5):1629–1640
Parker GA (1992) The evolution of sexual size dimorphism in fish. J Fish Biol 41(Suppl B):1–20
Peters RH (1983) The ecological implications of body size. Cambridge University Press, New York
Peters RH (1986) The ecological implications of body size. University Press, Cambridge (Cambridge Studies in Ecology, May 22, 1986)
Piersma T, Davidson KC (1991) Confusions of mass and size. Auk 108:441–444
Price TD, Grant PR, Gibbs HL, Boag PT (1984) Recurrent patterns of natural selection in a population of Darwin’s finches. Nature 309:787–789
Price TD (1984) The evolution of sexual size dimorphism in Darwin’s finches. Am Nat 123:500–518
Ralls K (1976) Mammals in which females are larger than males. Q Rev Biol 51:245–276
Reeve JP, Fairbairn DF (1996) Sexual size dimorphism as a correlated response to selection on body size: an empirical test of the quantitative genetic model. Evolution 50:1927–1938
Reiss MJ (1986) Sexual dimorphism in body size: are larger species more dimorphic? J Theor Biol 121:163–172
Rensch B (1960) Evolution above the species level. Columbia University Press, New York
Ricklefs RE, Cox GW (1977) Morphological similarity and ecological overlap among passerine birds on St. Kitts, British West Indies. Oikos 28:60–66
Ricklefs RE, Travis J (1980) A morphological approach to the study of avian community organization. Auk 97:321–338
Rising JD, Somers KM (1989) The measurement of overall body size in birds. Auk 106:666–674
Schmidt-Nielsen K (1984) Scaling. Why is animal size so important? Cambridge University Press, New York
Selander RK (1966) Sexual dimorphism and differential niche utilization in birds. Condor 68:113–151
Selander RK (1972) Sexual selection and dimorphism in birds. In: Campbell B (ed) Sexual selection and the descent of man1871–1971. Aldine Publ. Co., Chicago
Serrano-Meneses MA, Szekely T (2006) Sexual size dimorphism in seabirds: sexual selection, fecundity selection and differential niche-utilisation. Oikos 113:385–394
Shine R (1979) Sexual selection and sexual dimorphism in the Amphibia. Copeia 2:297–306
Shine R (1988) The evolution of large body size in females: a critique of Darwin’s “fecundity advantage” model. Am Nat 131:124–131
Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64:419–461
Slatkin M (1984) Ecological causes of sexual dimorphism. Evolution 38:622–630
Snow BK (1966) Observations on the behaviour and ecology of the Flightless Cormorant Nannopterum harrisi. Ibis 108:265–280
Snow DW, Nelson JB (1984) Evolution and adaptations of Galapagos sea-birds. Biol J Linn Soc 21:137–155
Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman and Company, New York
Stephens PR, Wiens JJ (2008) Testing for evolutionary tradeoffs in a phylogenetic context: ecological diversification and evolution of locomotor performance in emydid turtles. J Evol Biol 21:77–87
Stephens PR, Wiens JJ (2009) Evolution of sexual size dimorphisms in emydid turtles: Ecological dimorphism, Rensch’s rule, and sympatric divergence. Evolution 63:910–925
Szekely T, Reynolds JD, Foguerola J (2000) Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of natural selection. Evolution 54:1404–1413
Szekely T, Freckleton RP, Reynolds JD, Southwood R (2004) Sexual selection explains Rensch’s rule of size dimorphism in shorebirds. Proc Natl Acad Sci U S A 101:12224–12227
Thorton I (1971) Darwin’s Islands: a natural history of the Galapagos. The Natural History Press, New York
Tindle R (1984) The evolution of breeding strategies in the Flightless cormorant (Nannopterum harrisi) of the Galapagos. Biol J Linn Soc 21:157–164
Valle CA (1994) The ecology and evolution of sequential polyandry in Galapagos cormorants, Ph.D. Dissertation. Princeton University, Princeton
Valle CA (1995) Effective population size and demography of the rare flightless Galapagos cormorant. Ecol Appl 5:601–617
Valle CA (2009) The Flightless cormorant: the evolution of female rule In: de Roy T (ed) Galapagos: preserving Darwin’s legacy. David Bateman Ltd., New York
Webster MS (1992) Sexual dimorphism, mating system, and body size in New World blackbirds (Icterinae). Evolution 46:1621–1641
White EP, Morgan SK, Kerkhoff AJ, Enquist BJ (2007) Relationships between body size and abundance in ecology. Trends Ecol Evol 22:323–330
Wiens JA (1982) On size ratios and sequences in ecological communities: are there no rules? Ann Zool Fennici 19:297–308
Wikelski M (2005) Evolution of body size in Galapagos marine iguanas. Proc R Soc B 272:1985–1993
Wikelski M, Trillmich F (1997) Body size and sexual size dimorphism in marine iguanas fluctuate as a result of opposing natural and sexual selection: an island comparison. Evolution 51:922–936
Wiklund C, Karlsson B (1988) Sexual size dimorphism in relation to fecundity in some Swedish Satyrid butterflies. Am Nat 131:132–138
Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton
Wilson MF (1972) Seed size preference in finches. Wilson Bull 84:449–455
Wilson DS (1975) The adequacy of body size and a niche difference. Am Nat 109:769–784
Wilson RP, Vargas FH, Steinfurth A, Riordan P, Ropert-Coudert Y, MacDonald DW (2008) What grounds some birds for life? Movement and diving in the sexually dimorphic Galapagos cormorant. Ecol Monographs 78:633–652
Zeng Z-B (1988) Long-term correlated response, interpopulation covariation, and interspecific allometry. Evolution 42:363–374
Acknowledgments
I gratefully acknowledge financial support from Princeton University (Department of Ecology and Evolutionary Biology) and National Geographic that allowed me to conduct field research. I thank Universidad San Francisco de Quito and the Galapagos Academic Institute for the Arts and Sciences (GAIAS) through Santiago Gangotena (President), Carlos Montufar (Vice President), and Diego Quiroga (Dean for Scientific Research) for their encouragement and for allowing the necessary time for data analyses and preparing the manuscript for publication. I also thank Carlos Mena and Steve Walsh for their encouragement. I would like to thank John Krenz for his valuable comments and suggestions.
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Valle, C. (2013). Ecological Selection and the Evolution of Body Size and Sexual Size Dimorphism in the Galapagos Flightless Cormorant. In: Trueba, G., Montúfar, C. (eds) Evolution from the Galapagos. Social and Ecological Interactions in the Galapagos Islands, vol 2. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6732-8_12
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