The Role of Females in the Evolution of Sexual Dimorphism and Mating Systems

  • Chapter
  • First Online:
Ethology and Behavioral Ecology of Otariids and the Odobenid

Part of the book series: Ethology and Behavioral Ecology of Marine Mammals ((EBEMM))

  • 897 Accesses

Abstract

A hypothetical evolutionary process that may have given rise to sexual dimorphism and the mating system of pinnipeds was proposed half a century ago by Bartholomew (Evolution 24:546–559, 1970), yet it still remains the most accepted theory that links limited resources, body shape and behavior in the group (see Cassini, Chap. 6). Under this sexual selection approach, females are viewed as passive actors in the evolution of sexual characters and mating systems. The objective of this chapter is to propose a more active role of females in the evolutionary ecology of pinnipeds than that traditionally described. In this attempt to prioritize the role of females, the role of natural selection in the evolution of the sexual characteristics of these marine mammals becomes more relevant. The first section analyses the evolution of body size in pinnipeds, based on paleontological records, and describes the numerous advantages of large body size for a marine life. Each of the remaining four sections describe a different aspect of females that would have had an influence on the evolution of some unique pinniped trait. I argue that: (i) sexual size dimorphism skewed towards males can be explained by at least five different evolutionary mechanisms not related to sexual selection, (ii) that energy constraints of lactation has been an influential selective force that explains why phocids are on average significantly larger than otariids, (iii) that female avoidance of sexual disturbance is one of the most important determinant of the evolution of mating systems in pinnipeds, and (v) that mate choice by females has a more significant role in sexual selection than previously thought.

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

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Alexander RMN, Jayes AS, Maloiy GMO, Wathuta EM (1979) Allometry of limb bones of mammals from shrews (Sorex) to elephant (Loxodonta). J Zool Lond 189:305–314

    Article  Google Scholar 

  • Allainé D, Pontier D, Gaillard JM, Lebreton JD, Trouvilliez J, Clobert J (1987) The relationship between fecundity and adult body weight in homeotherms. Oecologia 73:478–480

    Article  PubMed  Google Scholar 

  • Andersson M (1994) Sexual selection, vol 72. Princeton University Press

    Google Scholar 

  • Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21(6):296–302

    Article  PubMed  Google Scholar 

  • Arnold SJ, Duvall D (1994) Animal mating systems: a synthesis based on selection theory. Am Nat 143(2):317–348

    Article  Google Scholar 

  • Bartholomew GA (1970) A model for the evolution of pinniped polygyny. Evolution 24:546–559

    Article  PubMed  Google Scholar 

  • Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2(3):349–368

    Article  CAS  PubMed  Google Scholar 

  • Berta A (1991) New Enaliarctos∗ (Pinnipedimorpha) from the Miocene of Oregon and the role of “Enaliarctids” in pinniped phylogeny. Smithson Contrib Paleobiol (69):1–32

    Google Scholar 

  • Berta A (2002) Pinniped evolution. In: Perrin WF, Wursig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, SanDiego, CA

    Google Scholar 

  • Berta A, Ray CE, Wyss AR (1989) Skeleton of the oldest known pinniped, Enaliarctos mealsi. Science 244:60–62

    Article  CAS  PubMed  Google Scholar 

  • Berta A, Sumich JL, Kovacs KM (2015) Marine mammals: Evolutionary biology, 3rd edn. Academic, San Diego, pp 35–58

    Book  Google Scholar 

  • Berta R, Churchill M, Boessenecker RW (2018) The origin and evolutionary biology of pinnipeds: seals, sea lions, and walruses. Annu Rev Earth Planet Sci 46:203–228

    Article  CAS  Google Scholar 

  • Bonnet X, Bradshaw SD, Shine R (1998) Capital versus income breeding: an ectothermic perspective. Oikos 83:333–341

    Article  Google Scholar 

  • Boyce MS (ed) (1988) Evolution of life histories of mammals: theory and pattern. Yale University Press, London

    Google Scholar 

  • Boyd I (2000) State-dependent fertility in pinnipeds: contrasting capital and income breeders. Funct Ecol 14:623–630

    Article  Google Scholar 

  • Campagna C, Le Boeuf BJ (1988) Reproductive behaviour of southern sea lions. Behaviour 104(3–4):233–261

    Article  Google Scholar 

  • Campagna C, Le Boeuf BJ, Cappozzo HL (1988a) Group raids: a mating strategy of male southern sea lions. Behaviour 105:224–249

    Article  Google Scholar 

  • Campagna C, Le Boeuf BJ, Cappozzo HL (1988b) Pup abduction and infanticide in southern sea lions. Behaviour 107:44–60

    Article  Google Scholar 

  • Campagna C, Bisioli C, Quintana F, Perez F, Vila A (1992) Group breeding in sea lions: pups survive better in colonies. Anim Behav 43(4):541–548

    Article  Google Scholar 

  • Cappozzo HL, Tunez JI, Cassini MH (2008) Sexual harassment and female gregariousness in the Southern Sea lion Otaria flavescens. Naturwissenschaften 95:625–630

    Article  CAS  PubMed  Google Scholar 

  • Cassini MH (1985) Comportamiento social de las hembras adultas del Lobo Marino del Sur, Otaria byronia (Blainville, 1820), durante la temporada de cría. Rev Latinoam Psicol 17:339–350

    Google Scholar 

  • Cassini MH (1999) The evolution of reproductive systems of pinnipeds. Behav Ecol 10:612–616

    Article  Google Scholar 

  • Cassini MH (2000) A model on female breeding dispersion and the reproductive systems of pinnipeds. Behav Process 51:93–99

    Article  CAS  Google Scholar 

  • Cassini MH (2011) Consequences of local Allee effects in spatially structured populations. Oecologia 165:547–552

    Article  PubMed  Google Scholar 

  • Cassini MH (2017) Role of fecundity selection on the evolution of size sexual dimorphism in mammals. Anim Behav 128:1–4

    Article  Google Scholar 

  • Cassini MH (2020) A mixed model of the evolution of polygyny and sexual size dimorphism in mammals. Mammal Rev 50:112–120

    Article  Google Scholar 

  • Cassini MH, Vilá BL (1990) Male mating behaviour of the southern sea lions. Bull Mar Sci 46(2):555–559

    Google Scholar 

  • Caudron AK, Negro SS, Fowler M, Boren L, Poncin P, Robertson BC, Gemmell NJ (2009) Alternative mating tactics in the New Zealand fur seal (Arctocephalus forsteri): when non-territorial males are successful too. Aust J Zool 57:409–421

    Google Scholar 

  • Charnov EL (1993) Life history invariants: some explorations of symmetry in evolutionary ecology, vol 6. Oxford University Press, USA

    Google Scholar 

  • Chilvers BL, Delean S, Gales NJ, Holley DK, Lawler IR, Marsh H, Preen AR (2004) Diving behaviour of dugongs, Dugong dugon. J Exp Mar Biol Ecol 304(2):203–224

    Article  Google Scholar 

  • Chilvers BL, Wilkinson IS, Duignan PJ, Gemmell NJ (2005) Summer foraging areas for lactating New Zealand sea lions Phocarctos hookeri. Mar Ecol Prog Ser 304:235–247

    Article  Google Scholar 

  • Churchill M, Clementz MT, Kohno N (2015) Cope’s rule and the evolution of body size in Pinnipedimorpha (Mammalia: Carnivora). Evolution 69(1):201–215

    Article  PubMed  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success. University Of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH, Harvey PH (1978) Mammals, resources and reproductive strategies. Nature 273:191–195

    Article  CAS  PubMed  Google Scholar 

  • Costa DP (1993, October) The relationship between reproductive and foraging energetics and the evolution of the Pinnipedia. Symp Zool Soc Lond 66:293–314

    Google Scholar 

  • Cullen TM, Fraser D, Rybczynski N, Schröder‐Adams C (2014) Early evolution of sexual dimorphism and polygyny in Pinnipedia. Evolution 68(5):1469–1484

    Article  PubMed  Google Scholar 

  • Darwin C (1874) The descent of man, and selection in relation to sex. John Murray, London

    Book  Google Scholar 

  • Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology. Wiley-Blackwell, Oxford

    Google Scholar 

  • Deméré TA, Berta A (2002) The pinniped Miocene Desmatophoca oregonensis Condon, 1906 (Mammalia: Carnivora) from the Astoria formation, Oregon. Smithson Contrib Paleobiol 93:113–147

    Google Scholar 

  • Dubuc C, Ruiz-Lambides A, Widding A (2014) Variance in male lifetime reproductive success and estimation of the degree of polygyny in a primate. Behav Ecol 25(4):878–889

    Article  PubMed  PubMed Central  Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197(4300):215–223

    Article  CAS  PubMed  Google Scholar 

  • Fay FH (1982) Ecology and biology of the Pacific walrus, Odobenus rosmarus divergens llliger. N Am Fauna 74:1

    Article  Google Scholar 

  • Francis JM (1987) Inter-female aggression and spacing in the northern fur seal, Callorhinus ursinus, and the California Sea lion, Zalophus californianus (PhD dissertation). University of California, Santa Cruz

    Google Scholar 

  • Fretwell SD, Lucas HL (1970) On territorial behaviour and other factors influencing habitat distribution in birds. Acta Biotheor 19:16–36

    Article  Google Scholar 

  • Fitzpatrick JL, Almbro M, Gonzalez-Voyer A, Kolm N, Simmons LW (2012) Male contest competition and the coevolution of weaponry and testes in pinnipeds. Evolution 66:3595–3604

    Article  PubMed  Google Scholar 

  • Flatz R, González-Suárez M, Young JK, Hernández-Camacho CJ, Immel AJ, Gerber LR (2012) Weak polygyny in California sea lions and the potential for alternative mating tactics. PLoS One 7:e33654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franco-Trecu V, Costa P, Schramm Y, Tassino B, Inchausti P (2014) Sex on the rocks: reproductive tactics and breeding success of South American fur seal males. Behav Ecol 25:1513–1523

    Article  Google Scholar 

  • Gemmell NJ, Burg TM, Boyd IL, Amos W (2001) Low RS in territorial male Antarctic fur seals (Arctocephalus gazella) suggests the existence of alternative mating strategies. Mol Ecol 10:451–460

    Article  CAS  PubMed  Google Scholar 

  • Goldsworthy SD, Boness DJ, Fleischer RC (1999) Mate choice among sympatric fur seals: female preference for conphenotypic males. Behav Ecol Sociobiol 45:253–267

    Article  Google Scholar 

  • Gonzalez-Suarez M, Cassini MH (2014) Variance in male RS and sexual size dimorphism in pinnipeds: testing an assumption of sexual selection theory. Mammal Rev 44:88–93

    Article  Google Scholar 

  • Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31(2):295–311

    Article  CAS  PubMed  Google Scholar 

  • Harcourt R (1992) Factors affecting mortality in the south American fur seal (Arctocephalus australis) in Peru: density-related effects and predation. J Zool (Lond) 226:259–270

    Article  Google Scholar 

  • Hoffman JI, Forcada J, Trathan PN, Amos W (2007) Female fur seals show active choice for males that are heterozygous and unrelated. Nature 445:912–914

    Article  CAS  PubMed  Google Scholar 

  • Houston AI, Stephens PA, Boyd IL, Harding KC, Mcnamara JM (2007) Capital or income breeding? A theoretical model of female reproductive strategies. Behav Ecol 18:241–250

    Article  Google Scholar 

  • Jones AG, Ratterman NL (2009) Mate choice and sexual selection: what have we learned since Darwin? PNAS 106:10001–10008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiyota M, Insley SJ, Lance S (2008) Effectiveness of territorial polygyny and alternative mating strategies in northern fur seals, Callorhinus ursinus. Behav Ecol Sociobiol 62:739–746

    Article  Google Scholar 

  • Krüger O, Wolf JBH, Jonker RM, Hoffman JI, Trillmich R (2014) Disentangling the contribution of sexual selection and ecology to the evolution of size dimorphism in pinnipeds. Evolution 68(5):1485–1496

    Article  PubMed  Google Scholar 

  • Lancaster ML, Gemmell NJ, Negro S, Goldsworthy S, Sunnucks P (2006) Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction. Mol Ecol 15(12):3681–3692

    Article  CAS  PubMed  Google Scholar 

  • Lancaster ML, Goldsworthy SD, Sunnucks P (2007a) Multiple mating strategies explain unexpected genetic mixing of New Zealand fur seals with two congenerics in a recently recolonized population. Mol Ecol 16(24):5267–5276

    Article  PubMed  Google Scholar 

  • Lancaster ML, Bradshaw CJ, Goldsworthy SD, Sunnucks P (2007b) Lower reproductive success in hybrid fur seal males indicates fitness costs to hybridization. Mol Ecol 16(15):3187–3197

    Article  CAS  PubMed  Google Scholar 

  • Le Boeuf BJ (1974) Male-male competition and reproductive success in elephant seals. Am Zool 14(1):163–176

    Article  Google Scholar 

  • Le Boeuf BJ, Briggs KT (1977) The cost of living in a seal harem. Mammalia 41:167–195

    Article  Google Scholar 

  • Lee PC, Majluf P, Gordon IJ (1991) Growth, weaning and maternal investment from a comparative perspective. J Zool (Lond) 225:99–114

    Article  Google Scholar 

  • Le Boeuf BJ, Crocker DE, Costa DP, Blackwell SB, Webb PM, Houser DS (2000) Foraging ecology of northern elephant seals. Ecol Monogr 70(3):353–382

    Article  Google Scholar 

  • Leutenegger W, Cheverud J (1982) Correlates of sexual dimorphism in primates: ecological and size variables. Int J Primatol 3:387–402

    Article  Google Scholar 

  • Lindenfors P (2002) Sexually antagonistic selection on primate size. J Evol Biol 15:595–607

    Article  Google Scholar 

  • Loison A, Gaillard JM, Pélabon C, Yoccoz NG (1999) What factors shape sexual size dimorphism in ungulates? Evol Ecol Res 1(5):611–633

    Google Scholar 

  • Marino L, Sol D, Thoren K, Lefebvre L (2006) Does diving limit brain size in cetaceans? Mar Mamm Sci 22:413–425

    Article  Google Scholar 

  • Marlow BJ (1975) The comparative behaviour of the Australasian sea lions Neophoca cinerea and Phocarctos hookeri (Pinnipedia: Otariidae). Mammalia 39(2):159–230

    Article  Google Scholar 

  • Mayr E (1963) Populations, species, and evolution. Belknap Press, Cambridge, MA

    Book  Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Article  Google Scholar 

  • Parker P, Maniscalco JM (2014) A long-term study reveals multiple reproductive behavior strategies among territorial adult male Steller sea lions (Eumetopias jubatus). Can J Zool 92(5):405–415

    Article  Google Scholar 

  • Purvis A, Harvey PH (1995) Mammal life-history evolution-a comparative test of Charnov’s model. J Zool (Lond) 237:259–283

    Article  Google Scholar 

  • Renouf D (1991) The behavior of pinnipeds. Chapman & Hall, New York, p 410

    Book  Google Scholar 

  • Repenning CA (1976) Adaptive evolution of sea lions and walruses. Syst Zool 25:375–390

    Article  Google Scholar 

  • Rogowitz GL (1996) Trade-offs in energy allocation during lactation. Am Zool 36:197–204

    Article  Google Scholar 

  • Schulz T, Bowen W (2005) The evolution of lactation strategies in pinnipeds: a phylogenetic analysis. Ecol Monogr 75:159–177. https://doi.org/10.1890/04-0319

  • Stirling I (1983) The evolution of mating systems in pinnipeds. Adv Study Mamm Behav 7:489–527

    Google Scholar 

  • Sjare B, Stirling I (2011) The breeding behavior of Atlantic walruses, Odobenus rosmarus rosmarus, in the Canadian high Arctic. Can J Zool 74(5):897–911

    Article  Google Scholar 

  • Slatkin M (1984) Ecological causes of sexual dimorphism. Evolution 38:622–630

    Article  PubMed  Google Scholar 

  • Soto KH, Trites AW (2011) South American sea lions in Peru have a lek-like mating system. Mar Mamm Sci 27:306–333

    Article  Google Scholar 

  • Trillmich F (1996) Parental investment in pinnipeds. In: Advances in the Study of Behavior, vol 25. Academic, pp 533–577

    Google Scholar 

  • Trillmich F, Trillmich KGK (1984) The mating systems of pinnipeds and marine iguanas: convergent evolution of polygyny. Biol J Linn Soc 21:209–216

    Article  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man, 1871–1971. Aldine-Atherton, Chicago, USA, pp 136–179

    Google Scholar 

  • Vaz-Ferreira R (1975) Behavior of the southern sea lion, Otaria flavescens (Shaw) in the Uruguayan islands. Rapp P-V Reun Cons Int Explor Mer 169:219–227

    Google Scholar 

  • Vilá BL, Cassini MH (1990) Aggressiveness between females and mother-pup separation in the southern sea lion, in Chubut, Argentina. Rev Chil Hist Nat 63:169–176

    Google Scholar 

  • Wade MJ (1979) Sexual selection and variance in reproductive success. Am Nat 114(5):742–747

    Article  Google Scholar 

  • Watts P, Hansen S, Lavigne DM (1993) Models of heat loss by marine mammals: thermoregulation below the zone of irrelevance. J Theor Biol 163(4):505–525

    Article  Google Scholar 

  • Weise MJ, Harvey JT, Costa DP (2010) The role of body size in individual-based foraging strategies of a top marine predator. Ecology 91:1004–1015

    Article  PubMed  Google Scholar 

  • Wyss AR (1994) The evolution of body size in phocids: some ontogenetic and phylogenetic observations. Proc San Diego Soc Nat Hist 29:69–75

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Cassini, M.H. (2021). The Role of Females in the Evolution of Sexual Dimorphism and Mating Systems. In: Campagna, C., Harcourt, R. (eds) Ethology and Behavioral Ecology of Otariids and the Odobenid. Ethology and Behavioral Ecology of Marine Mammals. Springer, Cham. https://doi.org/10.1007/978-3-030-59184-7_7

Download citation

Publish with us

Policies and ethics

Navigation