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Extra-pair paternity, sperm competition and the evolution of testis size in birds

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Abstract

Sperm competition should select for increased sperm production if the probability of fertilization by a specific male is proportional to the relative number of sperm inseminated. A review of the literature generally supports the predicted positive association between sperm production or allocation and various measures of the presumed intensity of sperm competition. However, it is not clear how increased sperm competition is related to extra-pair paternity, and it remains unknown whether certainty of paternity should be associated with relative testis size. Based on a large sample of bird species with information on extra-pair paternity gathered from the literature, we demonstrate that testis mass is related positively to the level of extra-pair paternity, after controlling for body size and phylogeny. Although large testes may be necessary to avoid sperm depletion in species in which males frequently engage in multi-pair copulations, we argue that selection has favoured increased testis mass in situations of more intense sperm competition in order to retaliate against copulations by rival males. The fact the males are not always successful in retaliating against rival ejaculates further suggests that females may largely control the allocation of paternity in birds and that increased sperm production by males may simply be a male strategy to make the best of a bad situation.

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References

  • Alatalo RV, Gustafsson L, Lundberg A (1984) High frequency of cuckoldry in pied and collared flycatchers. Oikos 42:41–47

    Google Scholar 

  • Alatalo RV, Gustafsson L, Lundberg A (1989) Extra-pair paternity and heritability estimates of tarsus length in pied and collared flycatchers. Oikos 56:54–58

    Google Scholar 

  • Birkhead TR, Fletcher F (1992) Sperm to spare? Sperm allocation by male zebra finches. Anim Behav 43:1053–1055

    Google Scholar 

  • Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic Press, London

    Google Scholar 

  • Birkhead TR, Pellatt J, Hunter FM (1988) Extra-pair copulation and sperm competition in the zebra finch. Nature 334:60–62

    Google Scholar 

  • Birkhead TR, Burke T, Zann R, Hunter FM, Krupa AP (1990) Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata revealed by DNA fingerprinting. Behav Ecol Sociobiol 27:315–324

    Google Scholar 

  • Birkhead TR, Hatehwell BJ, Davies NB (1991) Sperm competition and the reproductive organs of the male and female dunnock Prunella modularis. Ibis 133:306–311

    Google Scholar 

  • Birkhead TR, Briskie JV, Moller AP (1993) Male sperm reserves and copulation frequency in birds. Behav Ecol Sociobiol 32: 85–93

    Google Scholar 

  • Blakey JK (1989) Biochemical and population genetics in the great tit (Parus major). DPhil thesis, University of Oxford

  • Bollinger EK, Gavin TA (1991) Patterns of extra-pair fertilizations in bobolinks. Behav Ecol Sociobiol 29:1–7

    Google Scholar 

  • Briskie JV (1993a) Anatomical adaptations to sperm competition in Smith's longspurs and other polygynandrous passerines. Auk 110:875–888

    Google Scholar 

  • Briskie JV (1993b) Smith's longspur. In: Poole A, Stettenheim P, Gill F (eds) The birds of North America (no. 34). Academy of Natural Sciences, Philadelphia and American Ornithologists' Union, Washington

    Google Scholar 

  • Briskie JV, Montgomerie R (1993) Patterns of sperm storage in relation to sperm competition in passerine birds. Condor 95: 442–454

    Google Scholar 

  • Brooker MG, Rowley I, Adams M, Baverstock PR (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26:191–199

    Google Scholar 

  • Brown CR, Brown MB (1988) Genetic evidence of multiple parentage in broods of cliff swallows. Behav Ecol Sociobiol 23: 379–387

    Google Scholar 

  • Brownell RL Jr, Ralls K (1986) Potential for sperm competition in baleen whales. Rep Int Whaling Commission (special issue) 8:97–112

    Google Scholar 

  • Burke T (1989) DNA fingerprinting and other methods for the study of mating success. Trends Ecol Evol 4:139–144

    Google Scholar 

  • Burke T, Davies NB, Bruford MW, Hatchwell BJ (1989) Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature 338:249–251

    Google Scholar 

  • Burt A (1989) Comparative methods using phylogenetically independent contrasts. In: Harvey PH, Partridge L (eds) Oxford surveys in evolutionary biology, vol 6. Oxford University Press, Oxford, pp 33–53

    Google Scholar 

  • Cartar RV (1985) Testis size in sandpipers: the fertilization frequency hypothesis. Naturwissenschaften 72:157–158

    Google Scholar 

  • Glutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behaviour and ecology of two sexes. University of Chicago Press, Chicago

    Google Scholar 

  • Compton MM, Van Krey HP, Siegel PB (1978) The filling and emptying of the uterovaginal sperm-host glands in the domestic hen. Poult Sci 57:1696–1700

    Google Scholar 

  • Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B 205:489–511

    Google Scholar 

  • Dhondt AA (1991) How unreliable are cuckoldry estimates using heritability analyses? Ibis 133:91–93

    Google Scholar 

  • Dixon A, Ross D, O'Malley SLC, Burke T (1994) Paternal investment inversely related to degree of extra-pair paternity in the reed bunting. Nature 371:698–700

    Google Scholar 

  • Dunn PO, Robertson RJ (1993) Extra-pair paternity in polygynous tree swallows. Anim Behav 45:231–239

    Google Scholar 

  • Dunning JB Jr (1993) CRC handbook of avian body masses. CRC Press, Boca Raton

    Google Scholar 

  • Evarts S, Williams CJ (1987) Multiple paternity in a wild population of mallards. Auk 104:597–602

    Google Scholar 

  • Frumhoff PC, Reeve HK (1994) Using phylogenies to test hypotheses of adaptation: a critique of some current proposals. Evolution 48:172–180

    Google Scholar 

  • Gelter HP, Tegelstrom H (1992) High frequency of extra-pair paternity in Swedish pied flycatchers revealed by allozyme electrophoresis and DNA fingerprinting. Behav Ecol Sociobiol 31:1–7

    Google Scholar 

  • Gibbs HL, Weatherhead PJ, Boag PT, White BN, Tabak LM, Hoysak DJ (1990) Realized reproductive success of polygynous red-winged blackbirds revealed by DNA markers. Science 250: 1394–1397

    Google Scholar 

  • Ginsberg JR, Rubenstein DI (1990) Sperm competition and variation in zebra mating behavior. Behav Ecol Sociobiol 26: 427–434

    Google Scholar 

  • Grahn M (1992) Intra- and intersexual selection in the pheasant Phasianus colchicus. PhD thesis, Lund University

  • Graves J, Hay RT, Scallan M, Rowe S (1992) Extra-pair paternity in the shag, Phalacrocorax aristotelis as determined by DNA fingerprinting. J Zool 226:399–408

    Google Scholar 

  • Gullberg A, Tegelström H, Getter HP (1992) DNA fingerprinting reveals multiple paternity in families of great and blue tits (Parus major and P. caeruleus). Hereditas 117:103–108

    Google Scholar 

  • Gyllensten UB, Jakobsson S, Temrin H (1990) No evidence of illegitimate young in monogamous and polygynous warblers. Nature 343:168–170

    Google Scholar 

  • Harcourt AIL Harvey PH, Larson SG, Short RV (1981) Testes weight, body weight and breeding system in primates. Nature 293:55–57

    Google Scholar 

  • Hartley I, Shepherd M, Robson T, Burke T (1993) Reproductive success of polygynous male corn buntings (Miliaria calandra) as confirmed by DNA fingerprinting. Behav Ecol 4:310–317

    Google Scholar 

  • Harvey PH, Harcourt AH (1984) Sperm competition, testes size, and breeding systems in primates. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, Orlando, pp 589–600

    Google Scholar 

  • Harvey PH, Pagel M (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Heske EJ, Ostfeld RD (1990) Sexual dimorphism in size, relative size of testes, and mating systems in North American voles. J Mammal 71:510–519

    Google Scholar 

  • Hill GE, Montgomerie R, Roeder C, Boag P (1994) Sexual selection and cuckoldry in a monogamous songbird: implications for sexual selection theory. Behav Ecol Sociobiol 35:193–199

    Google Scholar 

  • Hoffenberg AS, Power HW, Romagnano LC, Lombardo MP, McGuire TR (1988) The frequency of cuckoldry in the European starling (Sturnus vulgaris). Wilson Bull 100:60–69

    Google Scholar 

  • Howard R, Moore A (1991) A complete checklist of the birds of the world (2nd edn). Academic Press, London

    Google Scholar 

  • Hunter FM, Burke TA, Watts SE (1992) Frequent copulation as a method of paternity assurance in the northern fulmar. Anim Behav 44:149–156

    Google Scholar 

  • Jennions MD, Passmore NI (1994) Sperm competition in frogs: testis size and a ‘sterile male’ experiment on Chiromantis xerampelina (Rhacophoridae). Biol J Linn Soc 50:211–220

    Google Scholar 

  • Johnston RF (1992) Rock dove. In: Poole A, Stettenheim P, Gill F (eds) The birds of North America (no 13). Academy of Natural Sciences, Philadelphia, and American Ornithologists' Union, Washington

    Google Scholar 

  • Jones CS, Lessells CM, Krebs JR (1991) Helpers-at-the-nest in European bee-eaters (Merops apiaster): a genetic analysis. In: Burke T, Dolf G, Jeffreys AJ, Wolff R (eds) DNA fingerprinting: approaches and applications. Birkhäuser Verlag, Basel, pp 169–172

    Google Scholar 

  • Kempenaers B, Verheyen GR, Broeck M van den, Burke T, Broeckhoven C van, Dhondt AA (1992) Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357:494–496

    Google Scholar 

  • Kenagy GJ, Trombulak SC (1986) Size and function of mammalian testes in relation to body size. J Mammal 67:1–22

    Google Scholar 

  • Kusano T, Toda M, Fukuyama K (1991) Testes size and breeding systems in Japanese anurans with special reference to large testes in the treefrog, Phacophorus arboretus (Amphibia: Thacophoridae). Behav Ecol Sociobiol 29:27–31

    Google Scholar 

  • Lank DB, Mineau P, Rockwell RF, Cooke F (1989) Intraspecific nest parasitism and extra-pair copulation in lesser snow geese. Anim Behav 37:74–89

    Google Scholar 

  • Lessells CM, Birkhead TR (1990) Mechanisms of sperm competition in birds: mathematical models. Behav Ecol Sociobiol 27:325–337

    Google Scholar 

  • Lifjeld JT, Dunn PO, Robertson RJ, Boag PT (1993) Extra-pair paternity in monogamous tree swallows. Anim Behav 45:213–229

    Google Scholar 

  • Lifjeld JT, Slagsvold T (1989) How frequent is cuckoldry in pied flycatchers Ficedula hypoleuca? Problems with the use of heritability estimates of tarsus length. Oikos 54:205–210

    Google Scholar 

  • Lifjeld JT, Slagsvold T, Lampe H (1991) Low frequency of extra-pair paternity in pied flycatchers revealed by DNA fingerprinting. Behav Ecol Sociobiol 29:95–101

    Google Scholar 

  • Marchant S, Higgins PJ (1990) Handbook of Australian, New Zealand and Antarctic birds (vol 1, part B). Oxford University Press, Melbourne

    Google Scholar 

  • Martin PA, Dziuk PJ (1977) Assessment of relative fertility of males (cockerels and boars). J Reprod Fert 49:323–329

    Google Scholar 

  • Martin PA, Reimers TJ, Lodge JR, Dziuk PJ (1974) The effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. J Reprod Fert 39:251–258

    Google Scholar 

  • Møller AP (1988a) Testes size, ejaculate quality, and sperm competition in birds. Biol J Linn Soc 33:273–283

    Google Scholar 

  • Møller AP (1988b) Ejaculate quality, testes size and sperm competition in primates. J Human Evol 17:479–488

    Google Scholar 

  • Møller AP (1989a) Frequency of extra-pair paternity in birds estimated from sex-differential heritability of tarsus length: reply to Lifjeld and Slagsvold's critique. Oikos 56:247–249

    Google Scholar 

  • Møller AP (1989b) Ejaculate quality, testes size and sperm production in mammals. Funct Ecol 3:91–96

    Google Scholar 

  • Møller AP (1991) Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am Nat 137:882–906

    Google Scholar 

  • Møller AP, Birkhead TR (1992a) Validation of the heritability method to estimate extra-pair paternity in birds. Oikos 64:485–488

    Google Scholar 

  • Møller AP, Birkhead TR (1992b) A pairwise comparative method as illustrated by copulation frequency in birds. Am Nat 139:644–656

    Google Scholar 

  • Møller AP, Birkhead TR (1994) The evolution of plumage brightness in birds is related to extrapair paternity. Evolution 48:1089–1100

    Google Scholar 

  • Mulder RA (1992) Evolutionary ecology of the mating system of superb fairy-wrens. PhD thesis, Australian National University, Canberra

    Google Scholar 

  • Mulder RA, Cockburn A (1993) Sperm competition and the reproductive anatomy of male superb fairy-wrens. Auk 110:588–593

    Google Scholar 

  • Mulder RA, Dunn PO, Cockburn A, Lazenby-Cohen KA, Howell MJ (1994) Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc R Soc Lond B 255:223–229

    Google Scholar 

  • Mumme RL, Koenig WD, Zink RM, Marten JA (1985) Genetic variation and parentage in a California population of acorn woodpeckers. Auk 102:305–312

    Google Scholar 

  • Olsen PD (1991) Do large males have small testes? A note on allometric variation and sexual size dimorphism in raptors. Oikos 60:134–136

    Google Scholar 

  • Oring LW, Fleischer RC, Reed JM, Marsden KE (1992) Cuckoldry through stored sperm in the sequentially polyandrous spotted sandpiper. Nature 359:631–633

    Google Scholar 

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

    Google Scholar 

  • Parker GA (1984) Sperm competition and the evolution of animal mating strategies. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, Orlando, pp 1–60

    Google Scholar 

  • Parker GA (1990) Sperm competition games: raffles and roles. Proc R Soc Lond B 242:120–126

    Google Scholar 

  • Payne RB, Payne LL (1989) Heritability estimates and behaviour observations: extra-pair matings in indigo buntings. Anim Behav 38:457–467

    Google Scholar 

  • Pinxten R, Hanotte O, Eens M, Verheyen RF, Dhondt AA, Burke T (1993) Extra-pair paternity and intraspecific brood parasitism in the European starling, Sturnus vulgaris: evidence from DNA fingerprinting. Anim Behav 45:795–809

    Google Scholar 

  • Purvis A (1991) Comparative analysis by independent contrasts, version 1.2: user's guide. Oxford University, Oxford

    Google Scholar 

  • Quinn JS, Woolfenden GE, Fitzpatrick JM, White BN (1990) DNA fingerprinting analysis of Florida shrub jay parentage. Do helpers help themselves? Abstracts, 108th Meeting of the American Ornithologist's Union, 29 June 1990, University of California, Los Angeles

    Google Scholar 

  • Riley HT, Bryant DM, Carter RE, Parkin DT (1995) Extra-pair fertilizations and paternity defence in house martins Delichon urhica. Anim Behav 49:495–509

    Google Scholar 

  • Schulze-Haven K, Swatschek I, Dyrcz A, Wink M (1993) Multiple Vaterschaften in Bruten des Seggenrorhsängers Acrocephalus paludicola: erste Ergebnisse des DNA-Fingerprintings. J Ornithol 134:145–154.

    Google Scholar 

  • Sheldon BC, Burke T (1994) Copulation behavior and paternity in the chaffinch. Behav Ecol Sociobiol 34:149–156

    Google Scholar 

  • Sherman PW, Morton ML (1988) Extra-pair fertilizations in mountain white-crowned sparrows. Behav Ecol Sociobiol 22:413–420

    Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New Haven and London

    Google Scholar 

  • Smith HG, Schantz T von (1993) Extra-pair paternity in the European starling: the effect of polygyny. Condor 95: 1006–1015

    Google Scholar 

  • Smith JNM, Zach R (1979) Heritability of some morphological characters in a song sparrow population. Evolution 33:460–467

    Google Scholar 

  • Smith HG, Montgomerie R, Põldmaa T, White BN, Boag PT (1991) DNA fingerprinting reveals relation between tail ornaments and cuckoldry in barn swallows, Hirundo rustica. Behav Ecol 2: 90–98

    Google Scholar 

  • Sodhi NS, Oliphant LW, James PC, Warkentin IG (1993) Merlin (Falco columharius). In: Poole A, Gill F (eds) The birds of North America (no 44). Academy of Natural Sciences, Philadelphia, and American Ornithologists' Union, Washington

    Google Scholar 

  • Svärd L, Wiklund C (1989) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24:395–402

    Google Scholar 

  • Triggs S, Williams M, Marshall S, Chambers G (1991) Genetic relationships within a population of blue duck Hymenolaimus malaorhynchos. Wildfowl 42:87–93

    Google Scholar 

  • Wedell N (1994) Spermatophore size in bushcrickets: comparative evidence for nuptial gifts as sperm protection device. Evolution 47:1203–1212

    Google Scholar 

  • Westneat DF (1987) Extra-pair fertilizations in a predominantly monogamous bird: genetic evidence. Anim Behav 35:877–886

    Google Scholar 

  • Westneat DF (1990) Genetic parentage in indigo buntings: a study using DNA fingerprinting. Behav Ecol Sociobiol 27:67–76

    Google Scholar 

  • Westneat DF (1992) Polygyny and extra-pair fertilizations in eastern red-winged blackbirds (Agelaius phocniceus). Behav Ecol 4: 49–60

    Google Scholar 

  • Wetton JH, Parkin DT (1991) An association between fertility and cuckoldry in the house sparrow, Passer domesticus. Proc R Soc Lond B 245:227–233

    Google Scholar 

  • Winge Ø (1937) Succession of broods in Lehistes. Nature 140:467

    Google Scholar 

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Moller, A.P., Briskie, J.V. Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav Ecol Sociobiol 36, 357–365 (1995). https://doi.org/10.1007/BF00167797

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