Skip to main content
SpringerLink
Log in

Geographical variation in sperm morphology in the red-winged blackbird (Agelaius phoeniceus)

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Many species differ genetically, physiologically, and morphologically between geographically distinct populations, typically in response to variation in ecological and climatic variables. Little is known, however, about geographical variation in sperm morphology. Sperm morphology is under strong sexual selection, has been shown to evolve rapidly, and often co-varies with other reproductive traits (e.g., testis size or mating system) that differ between populations in some species. The aim of this study was to establish whether sperm morphology varies between populations of the red-winged blackbird (Agelaius phoeniceus), a species with an enormous breeding range and marked inter-population variation in both body size and mating system. We found (1) highly significant variation in sperm morphology among study sites, (2) a gradual increase in sperm length from the southwest to the northeast of the breeding range, and (3) a strong negative association between sperm length and body size. However, the relationship with the mating system remains unclear. Several hypotheses to explain these patterns are proposed.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen JP, Hamon JH, McFarlane RW (1967) Some studies of the spermatozoa of certain species of the Icteridae (Blackbirds). Proc Indiana Acad Sci 77:434–441

    Google Scholar 

  • Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol Evol 12:235–239

    Article  CAS  PubMed  Google Scholar 

  • Ball RM Jr, Freeman S, James FC, Bermingham E, Avise JC (1988) Phylogeographic population structure of red-winged blackbirds assessed by mitochondrial DNA. Proc Natl Acad Sci USA 85:1558–1562

    Article  CAS  PubMed  Google Scholar 

  • Balshine S, Leach BJ, Neat F, Werner NY, Montgomerie R (2001) Sperm size of African cichlids in relation to sperm competition. Behav Ecol 12:726–731

    Article  Google Scholar 

  • Banerjee S, Carlin BP, Gelfand AE (2004) Hierarchical modeling and analysis for spatial data. Chapman & Hall/CRC, Boca Raton

    Google Scholar 

  • Beletsky L (1996) The red-winged blackbird. The biology of a strongly polygynous songbird. Academic Press, London

    Google Scholar 

  • Bergmann C (1847) Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien 1:595–708

    Google Scholar 

  • Birkhead TR, Biggins JD (1987) Reproductive synchrony and extra-pair copulation in birds. Ethology 74:320–334

    Article  Google Scholar 

  • Birkhead TR, Martínez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764

    Article  CAS  Google Scholar 

  • Birkhead TR, Pellatt EJ, Brekke P, Yeates R, Castillo-Juarez H (2005) Genetic effects on sperm design in the zebra finch. Nature 434:383–387

    Article  CAS  PubMed  Google Scholar 

  • Björklund M (1991) Evolution, phylogeny, sexual dimorphism and mating system in the grackles (Quiscalus spp.: Icterinae). Evolution 45:608–621

    Article  Google Scholar 

  • Blake (1968) Family Icteridae. In: Paynter RA Jr (ed) Check-list of birds of the world, vol XIV. Museum of Comparative Zoology, Harvard University, Cambridge, pp 138–202

    Google Scholar 

  • Blanckenhorn WU, Demont M (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr Comp Biol 44:413–424

    Article  PubMed  CAS  Google Scholar 

  • Blanckenhorn WU, Hellriegel B (2002) Against Bergmann’s rule: fly sperm size increases with temperature. Ecol Lett 5:7–10

    Article  Google Scholar 

  • Briskie JV, Montgomerie R (1992) Sperm size and sperm competition in birds. Proc R Soc Lond B 247:89–95

    Article  CAS  Google Scholar 

  • Briskie JV, Montgomerie R, Birkhead TR (1997) The evolution of sperm size in birds. Evolution 51:937–945

    Article  Google Scholar 

  • Burrows WH, Quinn JP (1937) The collection of spermatozoa from domestic fowl and turkey. Poult Sci 16:19–24

    Google Scholar 

  • Byrne PG, Simmons LW, Roberts JD (2003) Sperm competition and the evolution of gamete morphology in frogs. Proc R Soc Lond B 270:2079–2086

    Article  Google Scholar 

  • Calhim S, Birkhead TR (2007) Testes size in birds: quality versus quantity—assumptions, errors, and estimates. Behav Ecol 18:271–275

    Article  Google Scholar 

  • Calhim S, Immler S, Birkhead TR (2007) Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS ONE 2:e413. doi:10.1371/journal.pone.0000413

    Article  PubMed  Google Scholar 

  • Cornwallis CK, Birkhead TR (2007) Changes in sperm quality and numbers in response to experimental manipulation of male social status and female attractiveness. Am Nat 170:758–770

    Article  PubMed  Google Scholar 

  • Cummins JM, Woodall PF (1985) On mammalian sperm dimensions. J Reprod Fertil 75:153–175

    Article  CAS  PubMed  Google Scholar 

  • Dolbeer WA (1978) Movement and migration patterns of red-winged blackbirds: a continental overview. Bird Band 49:17–34

    Article  Google Scholar 

  • Dziminski MA, Roberts JD, Beveridge M, Simmons LW (2010) Among-population covariation between sperm competition and ejaculate expenditure in frogs. Behav Ecol 21:322–328

    Article  Google Scholar 

  • Elgee KE, Evans JP, Ramnarine IW, Rush SA, Pitcher TE (2010) Geographic variation in sperm traits reflects predation risk and natural rates of multiple paternity in the guppy. J Evol Biol 23:1331–1338

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Emslie SD (1998) Avian community, climate, and sea-level changes in the Plio-Pleistocene of the Florida Peninsula. Ornithol Monogr 50:1–113

    Google Scholar 

  • Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton

    Google Scholar 

  • Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc Natl Acad Sci USA 106:1128–1132

    Article  CAS  PubMed  Google Scholar 

  • Gage MJG (1994) Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc R Soc Lond B 258:247–254

    Article  Google Scholar 

  • Garrido O, Kirkconnell A (1996) Taxonomic status of the Cuban form of the red-winged blackbird. Wilson Bull 108:372–374

    Google Scholar 

  • Gavin TA, Howard RA, May B (1991) Allozyme variation among breeding populations of red-winged blackbirds: the California conundrum. Auk 108:602–611

    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

    Article  CAS  PubMed  Google Scholar 

  • Gomendio M, Roldan ERS (2008) Implications of diversity in sperm size and function for sperm competition and fertility. Int J Dev Biol 52:439–447

    Article  PubMed  Google Scholar 

  • Gould SJ, Johnston RF (1972) Geographic variation. Annu Rev Ecol Syst 3:457–498

    Article  Google Scholar 

  • Gray EM (1996) Female control of offspring paternity in a western population of red-winged blackbirds (Agelaius phoeniceus). Behav Ecol Sociobiol 38:267–278

    Article  Google Scholar 

  • Gray EM (1997a) Do female red-winged blackbirds benefit genetically from seeking extra-pair copulations? Anim Behav 53:605–623

    Article  Google Scholar 

  • Gray EM (1997b) Intraspecific variation in extra-pair behavior of red-winged blackbirds (Agelaius phoeniceus). Ornithol Monogr 49:61–80

    Google Scholar 

  • Hettyey A, Roberts JD (2006) Sperm traits of the quacking frog, Crinia georgiana: intra- and interpopulation variation in a species with a high risk of sperm competition. Behav Ecol Sociobiol 59:389–396

    Article  Google Scholar 

  • Hill GE (1994) Geographic variation in male ornamentation and female mate preference in the house finch: a comparative test of models of sexual selection. Behav Ecol 5:64–73

    Article  Google Scholar 

  • Holwell GI (2008) Geographic variation in genital morphology of Ciulfina praying mantids. J Zool 276:108–114

    Article  Google Scholar 

  • Hosken DJ, Garner TWJ, Blanckenhorn WU (2003) Asymmetry, testis and sperm size in yellow dung flies. Funct Ecol 17:231–236

    Article  Google Scholar 

  • Howell AH, van Rossem AJ (1928) A study of the red-winged blackbirds of souteasthern United States. Auk 45:155–163

    Google Scholar 

  • Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309

    Article  CAS  PubMed  Google Scholar 

  • Immler S, Birkhead TR (2005) A non-invasive method for obtaining spermatozoa from birds. Ibis 147:827–830

    Article  Google Scholar 

  • James FC (1970) Geographic variation in birds and its relationship to climate. Ecology 51:3

    Article  Google Scholar 

  • James FC (1983) Environmental component of morphological differentiation in birds. Science 221:184–186

    Article  CAS  PubMed  Google Scholar 

  • Jaramillo A, Burke P (1999) New World blackbirds: the icterids. Helm, London

    Google Scholar 

  • Kiefer MC, Van Sluys M, Rocha CFD (2008) Clutch and egg size of the tropical lizard Tropidurus torquatus (Tropiduridae) along its geographic range in coastal eastern Brazil. Can J Zool 86:1376–1388

    Article  Google Scholar 

  • Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT (2009) Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63:2466–2473

    Article  PubMed  Google Scholar 

  • Klicka J, Zink RM (1997) The importance of recent ice ages in speciation: a failed paradigm. Science 277:1666–1668

    Article  CAS  Google Scholar 

  • Kuramoto M (1996) Generic differentiation of sperm morphology in treefrogs from Japan and Taiwan. J Herpetol 30:437–443

    Article  Google Scholar 

  • Lack D (1947) Significance of clutch-size, parts I and II. Ibis 89:302–552

    Article  Google Scholar 

  • Legendre P (2000) Comparison of permutation methods for the partial correlation and partial Mantel tests. J Stat Comput Simul 67:37–73

    Article  Google Scholar 

  • Legendre P, Fortin M-J (1989) Spatial pattern and ecological analysis. Vegetatio 80:107–138

    Article  Google Scholar 

  • Lüpold S, Calhim S, Immler S, Birkhead TR (2009a) Sperm morphology and sperm velocity in passerine birds. Proc R Soc Lond B 276:1175–1181

    Article  Google Scholar 

  • Lüpold S, Linz GM, Birkhead TR (2009b) Sperm design and variation in the New World blackbirds (Icteridae). Behav Ecol Sociobiol 63:899–909

    Article  Google Scholar 

  • Lüpold S, Linz GM, Rivers JW, Westneat DF, Birkhead TR (2009c) Sperm competition selects beyond relative testes size in birds. Evolution 63:391–402

    Article  PubMed  Google Scholar 

  • Macedo RH, Karubian J, Webster MS (2008) Extrapair paternity and sexual selection in socially monogamous birds: are tropical birds different? Auk 125:769–777

    Article  Google Scholar 

  • Manier MK, Palumbi SR (2008) Intraspecific divergence in sperm morphology of the green sea urchin, Strongylocentrotus droebachiensis: implications for selection in broadcast spawners. BMC Evol Biol 8:283. doi:10.1186/1471-2148-8-283

    Article  PubMed  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • McFarlane RW (1963) The taxonomic significance of avian sperm. Proc XIII Int Ornithol Congr 91:91–102

    Google Scholar 

  • Miller GT, Pitnick S (2002) Sperm-female coevolution in Drosophila. Science 298:1230–1233

    Article  CAS  PubMed  Google Scholar 

  • Minoretti N, Baur B (2006) Among- and within-population variation in sperm quality in the simultaneously hermaphroditic land snail Arianta arbustorum. Behav Ecol Sociobiol 60:270–280

    Article  Google Scholar 

  • Møller AP (1995) Sexual selection in the barn swallow (Hirundo rustica). V. Geographic variation in ornament size. J Evol Biol 8:3–19

    Article  Google Scholar 

  • Moore WS, Dolbeer WA (1989) The use of banding recovery data to estimate dispersal rates and gene flow in avian species: case studies in the red-winged blackbird and common grackle. Condor 91:242–253

    Article  Google Scholar 

  • Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23

    CAS  PubMed  Google Scholar 

  • Morrow EH, Gage MJG (2001a) Artificial selection and heritability of sperm length in Gryllus bimaculatus. Heredity 87:356–362

    Article  CAS  PubMed  Google Scholar 

  • Morrow EH, Gage MJG (2001b) Consistent significant variation between individual males in spermatozoal morphometry. J Zool 254:147–153

    Article  Google Scholar 

  • Mossman J, Slate J, Humphries S, Birkhead TR (2009) Sperm morphology and velocity are genetically co-determined in the zebra finch. Evolution 63:2730–2737

    Article  PubMed  Google Scholar 

  • Murton RK, Westwood NJ (1977) Avian breeding cycles. Clarendon Press, Oxford

    Google Scholar 

  • Orians GH (1980) Some adaptations of marsh-nesting blackbirds. Princeton University Press, Princeton

    Google Scholar 

  • Parapanov R, Nusslé S, Hausser J, Vogel P (2008) Relationships of basal metabolic rate, relative testis size and cycle length of spermatogenesis in shrews (Mammalia, Soricidae). Reprod Fertil Dev 20:431–439

    Article  PubMed  Google Scholar 

  • Parker GA (1990) Sperm competition games: sneaks and extra-pair copulations. Proc R Soc Lond B 242:127–133

    Article  Google Scholar 

  • Parker GA (1993) Sperm competition games: sperm size and sperm number under adult control. Proc R Soc Lond B 253:245–254

    Article  CAS  Google Scholar 

  • Parker GA, Immler S, Pitnick S, Birkhead TR (2010) Sperm competition games: sperm size (mass) and number under raffle and displacement, and the evolution of P2. J Theor Biol 264:1003–1023

    Article  CAS  PubMed  Google Scholar 

  • Pellatt EJ, Birkhead TR (1994) Ejaculate size in zebra finches Taeniopygia guttata and a method for obtaining ejaculates from passerine birds. Ibis 136:97–106

    Article  Google Scholar 

  • Pitcher TE, Stutchbury BJM (1998) Latitudinal variation in testis size in six species of North American songbirds. Can J Zool 76:618–622

    Article  Google Scholar 

  • Pitnick S, Miller GT, Schneider K, Markow TA (2003) Ejaculate-female coevolution in Drosophila mojavensis. Proc R Soc Lond B 270:1507–1512

    Article  Google Scholar 

  • Pitnick S, Hosken DJ, Birkhead TR (2009) Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Elsevier, London, pp 69–149

    Google Scholar 

  • Pizzari T, Cornwallis CK, Froman D (2007) Social competitiveness associated with rapid fluctuations in sperm quality in male fowl. Proc R Soc Lond B 274:853–860

    Article  Google Scholar 

  • Podos J, Warren PS (2007) The evolution of geographic variation in birdsong. Adv Study Behav 37:403–458

    Article  Google Scholar 

  • Power DM (1969) Evolutionary implications of wing and size variation in the red-winged blackbird in relation to geographic and climatic factors: a multiple regression analysis. Syst Zool 18:363–373

    Article  Google Scholar 

  • Power DM (1970) Geographic variation of red-winged blackbirds in Central North America. Univ Kansas Publ Mus Nat Hist 19:1–83

    Google Scholar 

  • Prather JW, Cruz A (2006) Breeding biology of red-winged blackbirds in South Florida. Southeast Nat 5:547–554

    Article  Google Scholar 

  • Prevosti A, Serra L, Segarra E, Aguadé M, Ribó G, Monclús M (1990) Clines of chromosomal arrangements of Drosophila subobscura in South America evolve closer to old world patterns. Evolution 44:218–221

    Article  Google Scholar 

  • Ramm SA, Stockley P (2010) Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol Lett 6:219–221

    Article  PubMed  Google Scholar 

  • Rezende EL, Swanson DL, Fernando Novoa F, Bozinovic F (2002) Passerines versus nonpasserines: so far, no statistical differences in the scaling of avian energetics. J Exp Biol 205:101–107

    PubMed  Google Scholar 

  • Roff DA (1992) The evolution of life histories: theory and analysis. Chapman & Hall, New York

    Google Scholar 

  • Rosenberg MS (2001) PASSaGE. Pattern analysis, spatial statistics, and geographic exegesis. www.passagesoftware.net, Tempe, Arizona

  • Samour JH, Smith CA, Moore HD, Markham JA (1986) Semen collection and spermatozoa characteristics in budgerigars (Melopsittacus undulatus). Vet Rec 118:397–399

    Article  CAS  PubMed  Google Scholar 

  • Searcy WA, Yasukawa K (1995) Polygyny and sexual selection in red-winged blackbirds. Princeton University Press, Princeton

    Google Scholar 

  • Short RV (1981) Sexual selection in man and the great apes. In: Graham CE (ed) Reproductive biology of the great apes. Academic Press, New York, pp 319–341

    Google Scholar 

  • Simon G (1997) An angular version of spatial correlations, with exact significance tests. Geogr Anal 29:267–278

    Article  Google Scholar 

  • Snook RR (2001) Absence of latitudinal clines in sperm characters in North American populations of Drosophila subobscura (Diptera: Drosophilidae). Pan-Pac Entomol 77:261–271

    Google Scholar 

  • Spottiswoode C, Møller AP (2004) Extrapair paternity, migration, and breeding synchrony in birds. Behav Ecol 15:41–57

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Stutchbury BJ, Morton ES (1995) The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132:675–690

    Article  Google Scholar 

  • Van Rossem AJ (1926) The California forms of Agelaius phoeniceus (Linnaeus). Condor 28:215–230

    Article  Google Scholar 

  • Weatherhead PJ (1979) Ecological correlates of monogamy in tundra-breeding savannah sparrows. Auk 96:391–401

    Google Scholar 

  • Weatherhead PJ (1995) Effects on female reproductive success of familiarity and experience among male red-winged blackbirds. Anim Behav 49:967–976

    Article  Google Scholar 

  • Weatherhead PJ, Boag PT (1995) Pair and extra-pair mating success relative to male quality in red-winged blackbirds. Behav Ecol Sociobiol 37:81–91

    Article  Google Scholar 

  • Webster MS (1992) Sexual dimorphism, mating system and body size in New World blackbirds (Icterinae). Evolution 46:1621–1641

    Article  Google Scholar 

  • Westneat DF (1993a) Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav Ecol 4:49–60

    Article  Google Scholar 

  • Westneat DF (1993b) Temporal patterns of within-pair copulations, male mate guarding, and extra-pair events in eastern red-winged blackbirds (Agelaius phoeniceus). Behaviour 124:267–290

    Article  Google Scholar 

  • Westneat DF (2006) No evidence of current sexual selection on sexually dimorphic traits in a bird with high variance in mating success. Am Nat 167:E171–E189

    Article  Google Scholar 

  • Westneat DF, Mays HL (2005) Tests of spatial and temporal factors influencing extra-pair paternity in red-winged blackbirds. Mol Ecol 14:2155–2167

    Article  CAS  PubMed  Google Scholar 

  • Westneat DF, Sherman PW (1997) Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol 41:205–215

    Article  Google Scholar 

  • Westneat DF, McGraw LA, Fraterrigo JM, Birkhead TR, Fletcher F (1998) Patterns of courtship behavior and ejaculate characteristics in male red-winged blackbirds. Behav Ecol Sociobiol 43:161–171

    Article  Google Scholar 

  • Williams CL, Homan HJ, Johnston JJ, Linz GM (2004) Microsatellite variation in red-winged blackbirds (Agelaius phoeniceus). Biochem Genet 42:35–41

    Article  CAS  PubMed  Google Scholar 

  • Woolley DM (1971) Selection for the length of the spermatozoan midpiece in the mouse. Genet Res 16:261–275

    Article  Google Scholar 

  • Wright PL, Wright MH (1944) Reproductive cycle of the male red-winged blackbird. Condor 46:46–59

    Article  Google Scholar 

Download references

Acknowledgments

We thank J. Homan, G. Linz, L. Reinhardt, A. Trutsch, and K. Yasukawa for their help in the field, R. Byrd, J. Cummins, D. Elwonger, L. Merrill, T. Muir, J. Rivers, V. Rohwer, S. Tupper, S. Werner, and M. Whitfield for providing additional sperm samples, the SPU meeting at Syracuse University for insightful discussion, and R. Montgomerie, R. Snook and three anonymous reviewers for valuable comments on the manuscript. S.L. was supported by the Janggen-Poehn Foundation, Swiss National Science Foundation, a Sheffield University ORS Award, a Lauff Research Award, a KBS Visiting Graduate Student Fellowship, and an NSF LTER Graduate Research Award; D.F.W. by the University of Kentucky; and T.R.B. by the Leverhulme Trust.

Author information

Author notes

  1. Stefan Lüpold

    Present address: Department of Biology, Syracuse University, Life Sciences Complex, 107 College Place, Syracuse, NY, 13244-1270, USA

Authors and Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK

    Stefan Lüpold & Tim R. Birkhead

  2. Department of Biology, University of Kentucky, 101 Morgan Building, Lexington, KY, 40506, USA

    David F. Westneat

Authors
  1. Stefan Lüpold
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David F. Westneat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tim R. Birkhead
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefan Lüpold.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lüpold, S., Westneat, D.F. & Birkhead, T.R. Geographical variation in sperm morphology in the red-winged blackbird (Agelaius phoeniceus). Evol Ecol 25, 373–390 (2011). https://doi.org/10.1007/s10682-010-9410-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-010-9410-5

Keywords

Search

Navigation