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Laying-order effects on sperm numbers and on paternity: comparing three passerine birds with different life histories

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Abstract

In birds, the number of sperm trapped between the perivitelline membranes around the ovum is an estimate of sperm numbers present at the time and place of fertilisation in the female reproductive tract. Sperm numbers may vary among species and between eggs in a clutch and can provide information about sperm utilisation and mechanisms of sperm competition. Here, we describe patterns of variation in sperm numbers through the egg-laying sequence in three passerines in which extra-pair paternity is common, but copulation behaviour differs. Sperm numbers showed no systematic change across the laying sequence in blue tits (Cyanistes caeruleus), but decreased significantly with laying order in bluethroat (Luscinia svecica) and tree swallow (Tachycineta bicolor) clutches. This is consistent with observations that blue tits regularly copulate throughout the laying sequence, while bluethroats stop mate guarding and tree swallows reduce their copulation frequency once the first egg is laid. Nevertheless, cases of a sudden increase in sperm numbers in clutches of bluethroats and tree swallows suggest that successful inseminations also occurred after laying started. In blue tits and bluethroats, sperm numbers were not higher on extra-pair sired eggs than on eggs sired by the social male, suggesting that extra-pair copulations are not timed to the period of peak fertility for each egg. More extra-pair offspring originated from eggs laid early in the sequence in blue tits, while there was no systematic bias in bluethroats. Our results suggest that copulations during the laying sequence are predominantly performed by within-pair males in our study species.

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Acknowledgments

We thank Cheryl Bishop, Frode Fossøy, Karin Hieke, Terje Laskemoen, Anne Peters, Thomas Petitguyot, Angelika Poesel, Agnes Tuerk, Emmi Schlicht and Mihai Valcu for assistance in the field, and Frode Fossøy for lab assistance. We are grateful to Raphael-Thomas Klumpp and Alfred Fojt from the Institute of Silviculture, Vienna, for providing access to their facilities, to Hans Winkler from the Konrad Lorenz Institute for Comparative Ethology, Vienna, for logistical support, to the staff at the Queen’s University Biological Station for facilities and logistical support, and to Chris Eckert at Queens’ University for letting us use his microscopy laboratory. BK designed the study; KC and BK conducted the blue tit field work; AJ, KC, KD, JTL and BK conducted the bluethroat fieldwork; KC, RJR and BK conducted the tree swallow fieldwork; KC and BK counted the sperm on the egg membranes; KC conducted the blue tit paternity analysis, AJ conducted the bluethroat paternity analysis; AJ and BK analysed the data; AJ wrote the paper in collaboration with all other co-authors. We thank Jim Briskie and two anonymous reviewers for thoughtful comments on the manuscript. The work was funded by the Max Planck Society, the Norwegian research Council, the Natural History Museum of the University of Oslo, and the Natural Sciences and Engineering Research Council of Canada.

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The work described here was done under license and complied with the current laws of the countries in which it was performed.

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Authors and Affiliations

  1. National Centre for Biosystematics, Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, NO-0318, Oslo, Norway

    Arild Johnsen & Jan T. Lifjeld

  2. Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Eberhard Gwinnerstr, 82319, Starnberg (Seewiesen), Germany

    Kim L. Carter, Kaspar Delhey & Bart Kempenaers

  3. School of Biological Sciences, Monash University, Clayton, 3800, Victoria, Australia

    Kaspar Delhey

  4. Department of Biology, Queen’s University, Kingston, ON, K7L 3N6, Canada

    Raleigh J. Robertson

Authors
  1. Arild Johnsen
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  2. Kim L. Carter
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  3. Kaspar Delhey
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  4. Jan T. Lifjeld
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  5. Raleigh J. Robertson
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  6. Bart Kempenaers
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Corresponding author

Correspondence to Bart Kempenaers.

Additional information

Communicated by J. Graves

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Table S1

Paternity of eggs (○ = within-pair, ● = extra-pair) in relation to laying order in blue tits (DOC 43 kb)

Table S2

Paternity of eggs (○ = within-pair, ● = extra-pair, ? = unknown) in relation to laying order in bluethroats (DOC 44 kb)

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Johnsen, A., Carter, K.L., Delhey, K. et al. Laying-order effects on sperm numbers and on paternity: comparing three passerine birds with different life histories. Behav Ecol Sociobiol 66, 181–190 (2012). https://doi.org/10.1007/s00265-011-1265-4

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  • DOI: https://doi.org/10.1007/s00265-011-1265-4

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