Do ornaments, arrival date, and sperm size influence mating and paternity success in the collared flycatcher?

  • Anaïs Edme
  • Petr Zobač
  • Pavlína Opatová
  • Petra Šplíchalová
  • Pavel Munclinger
  • Tomáš Albrecht
  • Miloš Krist
Original Article

Abstract

Males advertise their intrinsic parental and/or genetic qualities by the size of secondary sexual ornaments. Moreover, they compete with one another for the best territory and males who arrive first at the breeding ground usually have an advantage in this competition. Females may consider multiple male qualities simultaneously and prefer the one most important for their fitness in the current context. They can further improve their fitness by selecting the best care-giver as their social mate and engaging in an extra-pair copulation with a genetically superior male. In such cases, sperm competition arises in the female reproductive tract and its outcome may be affected by the sperm morphology of both the social and extra-pair male. Here, we tested these ideas in the collared flycatcher (Ficedula albicollis), a species with context-dependent choice of social partners and frequent extra-pair paternity. We recorded male arrival to breeding sites, manipulated their forehead patches, and measured sperm size. In contrast to a previous study in a Swedish population, males with enlarged patches were non-significantly less successful late in the season while no such difference was found early in the season. Besides this tendential seasonal interaction, arrival date did not affect mating and paternity success or male fitness, and the same was true for sperm size. These results suggest different benefits of male ornamentation and female mate choice between populations and call for more replicated research within and between species.

Significance statement

The fitness of a male of a migratory species might be affected by several pathways. First, early arrival should confer benefits in the form of best territory choice. Second, in a dichromatic and sexually promiscuous species, secondary sexual ornaments are considered by females both in the choice of social and extra-pair mates. Third, by modifying sperm traits, males may outmatch their rivals in sperm competition. These ideas have usually been tested in isolation. In this experimental study, we tested the joint effect of all of these factors on the genetic fitness of males. We found little evidence for the dependence of male reproductive success on either sperm morphology or plumage ornamentation which is in contrast to other populations of the species. Our study calls for replicated research both in well-established fields like mate choice and emerging ones like sperm competition.

Keywords

Mating success Extra-pair paternity Differential allocation Sexual ornament Sperm size 

Supplementary material

265_2016_2242_MOESM1_ESM.docx (1.2 mb)
ESM 1(DOCX 1199 kb)

References

  1. Aebischer A, Perrin N, Krieg M, Studer J, Meyer DR (1996) The role of territory choice, mate choice and arrival date on breeding success in the Savi’s Warbler Locustella luscinioides. J Avian Biol 27:143–152CrossRefGoogle Scholar
  2. Akçay E, Roughgarden J (2007) Extra-pair paternity in birds : review of the genetic benefits. Evol Ecol Res 9:855–868Google Scholar
  3. Alatalo RV, Lundberg A, Glynn C (1986) Female pied flycatchers choose territory quality and not male characteristics. Nature 323:152–153CrossRefGoogle Scholar
  4. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  5. Beck ML (2013) Nest-box acquisition is related to plumage coloration in male and female prothonotary warblers (Protonotaria citrea). Auk 130:364–371CrossRefGoogle Scholar
  6. Bennison C, Hemmings N, Slate J, Birkhead T (2015) Long sperm fertilize more eggs in a bird. Proc R Soc B 282:20141897CrossRefPubMedPubMedCentralGoogle Scholar
  7. Birkhead TR, Hunter FM, Pellatt E (1989) Sperm competition in the zebra finch, Taeniopygia guttata. Anim Behav 38:935–950CrossRefGoogle Scholar
  8. Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764CrossRefGoogle Scholar
  9. Callander S, Backwell PRY, Jennions MD (2012) Context-dependent male mate choice: the effects of competitor presence and competitor size. Behav Ecol 23:355–360CrossRefGoogle Scholar
  10. Cleasby IR, Nakagawa S (2012) The influence of male age on within-pair and extra-pair paternity in passerines. Ibis 154:318–324CrossRefGoogle Scholar
  11. Cramer ERA, Laskemoen T, Kleven O, Lebarbera K, Lovette IJ, Lifjeld JT (2013) No evidence that sperm morphology predicts paternity success in wild house wrens. Behav Ecol Sociobiol 67:1845–1853CrossRefGoogle Scholar
  12. de Heij ME, Gustafsson L, Brommer JE (2011) Experimental manipulation shows that the white wing patch in collared flycatchers is a male sexual ornament. Ecol Evol 1:546–555CrossRefPubMedPubMedCentralGoogle Scholar
  13. Drăgănoiu TI, Nagle L, Kreutzer M (2002) Directional female preference for an exaggerated male trait in canary (Serinus canaria) song. Proc R Soc Lond B 269:2525–2531CrossRefGoogle Scholar
  14. Edme A, Munclinger P, Krist M (2016) Female collared flycatchers choose neighbouring and older extra-pair partners from the pool of males around their nests. J Avian Biol 47:552–562CrossRefGoogle Scholar
  15. Ellegren H (1992) Polymerase-chain-reaction (PCR) analysis of microsatellites—a new approach to studies of genetic relationships in birds. Auk 109:886–895CrossRefGoogle Scholar
  16. Garamszegi LZ, Rosivall B, Hegyi G, Szöllösi E, Török J, Eens M (2006) Determinants of male territorial behavior in a Hungarian collared flycatcher population: plumage traits of residents and challengers. Behav Ecol Sociobiol 60:663–671CrossRefGoogle Scholar
  17. Gentner TQ, Hulse SH (2000) Female European starling preference and choice for variation in conspecific male song. Anim Behav 59:443–458CrossRefPubMedGoogle Scholar
  18. Gibbs HL, Tabak LM, Hobson K (1999) Characterization of microsatellite DNA loci for a neotropical migrant songbird, the Swainson’s thrush (Catharus ustulatus). Mol Ecol 8:1551–1561CrossRefGoogle Scholar
  19. Grana SC, Sakaluk SK, Bowden RM, Doellman MA, Vogel LA, Thompson CF (2012) Reproductive allocation in female house wrens is not influenced by experimentally altered male attractiveness. Behav Ecol Sociobiol 66:1247–1258CrossRefGoogle Scholar
  20. Griffith SC, Owens IPF, Burke T (1999) Female choice and annual reproductive success favour less-ornamented male house sparrows. Proc R Soc Lond B 266:765–770CrossRefGoogle Scholar
  21. Gustafsson L, Qvarnström A, Sheldon BC (1995) Trade-offs between life history traits and a secondary sexual character in male collared flycatchers. Nature 375:311–313CrossRefGoogle Scholar
  22. Hale RE (2008) Evidence that context-dependent mate choice for parental care mirrors benefits to offspring. Anim Behav 75:1283–1290CrossRefGoogle Scholar
  23. Hegyi G, Török J, Toth L (2002) Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher. J Evol Biol 15:710–719CrossRefGoogle Scholar
  24. Horváthová T, Nakagawa S, Uller T (2012) Strategic female reproductive investment in response to male attractiveness in birds. Proc R Soc Lond B 279:163–170CrossRefGoogle Scholar
  25. Hoyt DF (1979) Practical methods of estimating volume and fresh weight of birds’ eggs. Auk 96:73–77Google Scholar
  26. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64CrossRefPubMedGoogle Scholar
  27. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  28. Kempenaers B, Verheyen G, Van den Broeck M, Burke T, Van Broeckhoven C, Dhondt A (1992) Extra-pair paternity results from female preference for high quality males in the blue tit. Nature 357:494–496CrossRefGoogle Scholar
  29. Krist M (2009) Short- and long-term effects of egg size and feeding frequency on offspring quality in the collared flycatcher (Ficedula albicollis). J Anim Ecol 78:907–918CrossRefPubMedGoogle Scholar
  30. Krist M, Munclinger P (2011) Superiority of extra-pair offspring: maternal but not genetic effects as revealed by a mixed cross-fostering design. Mol Ecol 20:5074–5091CrossRefPubMedGoogle Scholar
  31. Krist M, Nádvorník P, Uvírová L, Bureš S (2005) Paternity covaries with laying and hatching order in the collared flycatcher Ficedula albicollis. Behav Ecol Sociobiol 59:6–11CrossRefGoogle Scholar
  32. Laskemoen T, Kleven O, Fossøy F, Robertson RJ, Rudolfsen G, Lifjeld JT (2010) Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallow Tachycineta bicolor. Behav Ecol Sociobiol 64:1473–1483CrossRefGoogle Scholar
  33. Leder EH, Karaiskou N, Primmer CR (2008) Seventy new microsatellites for the pied flycatcher, Ficedula hypoleuca and amplification in other passerine birds. Mol Ecol Resour 8:874–880CrossRefPubMedGoogle Scholar
  34. Lifjeld JT, Slagsvold T, Ellegren H (1997) Experimental mate switching in pied flycatchers: male copulatory access and fertilization success. Anim Behav 53:1225–1232CrossRefPubMedGoogle Scholar
  35. Lifjeld JT, Laskemoen T, Kleven O, Albrecht T, Robertson RJ (2010) Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS One 5:e13456CrossRefPubMedPubMedCentralGoogle Scholar
  36. Mazuc J, Chastel O, Sorci G (2003) No evidence for differential maternal allocation to offspring in the house sparrow (Passer domesticus). Behav Ecol 14:340–346CrossRefGoogle Scholar
  37. Mitchell DP, Dunn PO, Whittingham LA, Freeman-Gallant CR (2007) Attractive males provide less parental care in two populations of the common yellowthroat. Anim Behav 73:165–170CrossRefGoogle Scholar
  38. Møller AP (2004) Protandry, sexual selection and climate change. Glob Change Biol 10:2028–2035CrossRefGoogle Scholar
  39. Møller AP, Birkhead TR (1993) Cuckoldry and sociality: a comparative study of birds. Am Nat 142:118–140CrossRefPubMedGoogle Scholar
  40. Mougeot F (2004) Breeding density, cuckoldry risk and copulation behaviour during the fertile period in raptors: a comparative analysis. Anim Behav 67:1067–1076CrossRefGoogle Scholar
  41. Pärt T, Qvarnström A (1997) Badge size in collared flycatchers predicts outcome of male competition over territories. Anim Behav 54:893–899CrossRefGoogle Scholar
  42. Quay WB (1986) Cloacal protuberance and cloacal sperm in passerine birds: comparative study of quantitative relations. Condor 88:160–168CrossRefGoogle Scholar
  43. Qvarnström A (1997) Experimentally increased badge size increases male competition and reduces male parental care in the collared flycatcher. Proc R Soc Lond B 264:1225–1231CrossRefGoogle Scholar
  44. Qvarnström A (1999) Different reproductive tactics in male collared flycatchers signalled by size of secondary sexual character. Proc R Soc Lond B 266:2089–2093CrossRefGoogle Scholar
  45. Qvarnström A (2001) Context-dependent genetic benefits from mate choice. Trends Ecol Evol 16:5–7CrossRefPubMedGoogle Scholar
  46. Qvarnström A, Pärt T, Sheldon BC (2000) Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature 405:344–347CrossRefPubMedGoogle Scholar
  47. R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
  48. Richardson DS, Burke T (1999) Extra-pair paternity in relation to male age in Bullock’s orioles. Mol Ecol 8:2115–2126CrossRefPubMedGoogle Scholar
  49. Rosivall B, Szöllösi E, Hasselquist D, Török J (2009) Effects of extrapair paternity and sex on nestling growth and condition in the collared flycatcher, Ficedula albicollis. Anim Behav 77:611–617CrossRefGoogle Scholar
  50. Scordato ESC, Safran RJ (2014) Geographic variation in sexual selection and implications for speciation in the Barn Swallow. Avian Res 5:8CrossRefGoogle Scholar
  51. Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402CrossRefPubMedGoogle Scholar
  52. Sheldon BC, Ellegren H (1999) Sexual selection resulting from extrapair paternity in collared flycatchers. Anim Behav 57:285–298CrossRefPubMedGoogle Scholar
  53. Sheldon BC, Merilä J, Qvarnström A, Gustafsson L, Ellegren H (1997) Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc R Soc Lond B 264:297–302CrossRefGoogle Scholar
  54. Smith CC (2012) Opposing effects of sperm viability and velocity on the outcome of sperm competition. Behav Ecol 23:820–826CrossRefGoogle Scholar
  55. Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53CrossRefPubMedGoogle Scholar
  56. Török J, Hegyi G, Garamszegi LZ (2003) Depigmented wing patch size is a condition-dependent indicator of viability in male collared flycatchers. Behav Ecol 14:382–388CrossRefGoogle Scholar
  57. Tottrup AP, Thorup K (2008) Sex-differentiated migration patterns, protandry and phenology in North European songbird populations. J Ornithol 149:161–167CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Anaïs Edme
    • 1
  • Petr Zobač
    • 1
  • Pavlína Opatová
    • 1
    • 2
    • 3
  • Petra Šplíchalová
    • 4
  • Pavel Munclinger
    • 4
  • Tomáš Albrecht
    • 2
    • 4
  • Miloš Krist
    • 1
    • 5
  1. 1.Department of Zoology and Laboratory of Ornithology, Faculty of SciencePalacký UniversityOlomoucCzech Republic
  2. 2.Institute of Vertebrate BiologyCzech Academy of SciencesBrnoCzech Republic
  3. 3.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  4. 4.Department of Zoology, Faculty of ScienceCharles University in PraguePragueCzech Republic
  5. 5.Museum of Natural HistoryOlomoucCzech Republic

Personalised recommendations