Volume 6 Issue 1
Jan.  2020
Turn off MathJax
Article Contents
Article Navigation >  Avian Research  > 2015  >  6: 23.
Melissah Rowe, Simon C. Griffith, Antje Hofgaard, Jan T. Lifjeld. 2015: Subspecific variation in sperm morphology and performance in the Long-tailed Finch (Poephila acuticauda). Avian Research, 6(1): 23. doi: 10.1186/s40657-015-0032-z
Citation: Melissah Rowe, Simon C. Griffith, Antje Hofgaard, Jan T. Lifjeld. 2015: Subspecific variation in sperm morphology and performance in the Long-tailed Finch (Poephila acuticauda). Avian Research, 6(1): 23. doi: 10.1186/s40657-015-0032-z
shu

Subspecific variation in sperm morphology and performance in the Long-tailed Finch (Poephila acuticauda)

doi: 10.1186/s40657-015-0032-z
  • 1.

    Natural History Museum, University of Oslo, PO Box 1172, Blindern, 0318 Oslo, Norway

  • 2.

    Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, PO Box 1066, Blindern, 0316 Oslo, Norway

  • 3.

    Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia

  • 4.

    Electron Microscopical Unit for Biological Sciences, Department of Biosciences, University of Oslo, PO Box 1041, Blindern, 0316 Oslo, Norway

More Information
  • Corresponding author: Melissah Rowe, melissah.rowe@nhm.uio.no
  • Received Date: 08 Jul 2015
  • Accepted Date: 15 Oct 2015
  • Publish Date: 01 Dec 2015
    Abstract
  • Background Evolutionary biology endeavours to explain biological diversity,and as such it is critical to develop an understanding of the adaptive and functional significance of trait variation. Spermatozoa exhibit remarkable levels of morphological diversification. However,our understanding of the evolutionary causes and functional significance of this variation is limited,especially at the intraspecific level.
    Methods We quantified variation in sperm morphology and performance between two subspecies of Long-tailed Finch (Poephila acuticauda acuticauda and P. a. hecki),a small grassfinch found in tropical northern Australia. Despite a zone of secondary contact,these subspecies are maintained as two distinct forms: P. a. acuticauda occurs in the western part of the species' range and has a yellow bill,while P. a. hecki exhibits a red bill and is found in the eastern part of the range.
    Results We found small,but significant differences in sperm size between these subspecies (P. a. acuticauda had longer and narrower sperm than P. a. hecki),which was surprising given the recent evolutionary origins of these two taxa (i.e. 0.3 million years ago). Additionally,both subspecies exhibited high values of between- and within-male variation in sperm morphology,though in the case of sperm midpiece length this variation was significantly lower in P. a. acuticauda relative to P. a. hecki.
    Conclusions We suggest these observed differences in sperm morphology are the result of genetic drift and reflect historical processes associated with divergence between the eastern and western populations of these two subspecies. Finally,we discuss the potential implications of our findings for the process of population divergence and reproductive isolation.

     

    • FullText(HTML)
  • loading
    • References(75)
  • Albrechtová J, Albrecht T, Baird SJE, Macholán M, Rudolfsen G, Munclinger P, Tucker PK, Piálek J. Sperm-related phenotypes implicated in both maintenance and breakdown of a natural species barrier in the house mouse. Proc R Soc B. 2012;279:4803-10. doi: 10.1098/rspb.2012.1802
    Bennison C, Hemmings N, Slate J, Birkhead T. Long sperm fertilize more eggs in a bird. Proc R Soc B. 2015;. doi: 10.1098/rspb.2014.1897.
    Birkhead TR, Martinez JG, Burke T, Froman DP. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc B. 1999;266:1759-64. doi: 10.1098/rspb.1999.0843
    Birkhead TR, Pellatt EJ, Brekke P, Yeates R, Castillo-Juarez H. Genetic effects on sperm design in the zebra finch. Nature. 2005;434:383-7. doi: 10.1038/nature03374
    Birkhead TR, Immler S, Pellatt EJ, Freckleton R. Unusual sperm morphology in the eurasian bullfinch (Pyrrhula pyrrhula). Auk. 2006;123:383-92. doi: 10.1093/auk/123.2.383
    Bowman DMJS, Brown GK, Braby MF, Brown JR, Cook LG, Crisp MD, Ford F, Haberle S, Hughes J, Isagi Y, Joseph L, McBride J, Nelson G, Ladiges PY. Biogeography of the Australian monsoon tropics. J Biogeog. 2010;37:201-16. doi: 10.1111/j.1365-2699.2009.02210.x
    Briskie JV, Montgomerie R. Patterns of sperm storage in relation to sperm competition in passerine birds. Condor. 1993;95:442-54. doi: 10.2307/1369366
    Briskie JV, Montgomerie R, Birkhead TR. The evolution of sperm size in birds. Evolution. 1997;51:937-45. doi: 10.1111/j.1558-5646.1997.tb03674.x
    Calhim S, Immler S, Birkhead TR. Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS One. 2007;2:e143. doi: 10.1371/journal.pone.0000143
    Cramer ERA, Laskemoen T, Stensrud E, Rowe M, Haas F, Lifjeld JT, Saetre G-P, Johnsen A. Morphology-function relationships and repeatability in the sperm of Passersparrows. J Morphol. 2015;276:370-7. doi: 10.1002/jmor.20346
    Cruz-Orive LM, Weibel ER. Recent stereological methods for cell biology: a brief survey. Am J Physiol. 1990;258:148-56. http://cn.bing.com/academic/profile?id=42c05ef9537979e1e54c9f53099e0932&encoded=0&v=paper_preview&mkt=zh-cn
    De Deckker P. Late quaternary cyclic aridity in tropical Australia. Palaeogeogr Palaeocl. 2001;170:1-9. doi: 10.1016/S0031-0182(01)00233-4
    Dean MD, Nachman MW. Faster fertilization rate in conspecific versus heterospecific matings in house mice. Evolution. 2009;63:20-8. doi: 10.1111/j.1558-5646.2008.00499.x
    Denk AG, Holzmann A, Peters A, Vermeirssen ELM, Kempenaers B. Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav Ecol. 2005;16:825-33. doi: 10.1093/beheco/ari065
    Fitzpatrick JL, Baer B. Polyandry reduces sperm length variation in social insects. Evolution. 2011;65:3006-12. doi: 10.1111/j.1558-5646.2011.01343.x
    Fitzpatrick JL, Lüpold S. Sexual selection and the evolution of sperm quality. Mol Hum Reprod. 2014;20:1180-9. doi: 10.1093/molehr/gau067
    Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S. Female promiscuity promotes the evolution of faster sperm in cichlid fishes. P Natl Acad Sci USA. 2009;106:1128-32. doi: 10.1073/pnas.0809990106
    Harcourt AH, Purvis A, Liles L. Sperm competition: mating system, not breeding season, affects testes size of primates. Funct Ecol. 1995;9:468-76. doi: 10.2307/2390011
    Helfenstein F, Podevin M, Richner H. Sperm morphology, swimming velocity, and longevity in the house sparrowPasser domesticus. Behav Ecol Sociobiol. 2010;64:557-65. doi: 10.1007/s00265-009-0871-x
    Hettyey A, Roberts JD. Sperm traits of the quacking frog, Crinia georgiana:Intra- and interpopulation variation in a species with a high risk of sperm competition. Behav EcolSociobiol. 2006;59:389-96.
    Higgins PJ, Peter JM, Cowling SJ. Handbook of Australian, New Zealand and Antarctic Birds. Boatbill to Starlings (vol. 7). Melbourne; Oxford University Press; 2006.
    Hogner S, Laskemoen T, Lifjeld JT, Pavel V, Chutný B, García J, Eybert M-C, Matsyna E, Johnsen A. Rapid sperm evolution in the bluethroat (Luscinia svecica) subspecies complex. Behav Ecol Sociobiol. 2013;67:1205-17.
    Hosken DJ. Sperm competition in bats. Proc R Soc B. 1997;264:385-92. doi: 10.1098/rspb.1997.0055
    Hosken DJ, Garner TWJ, Blanckenhorn WU. Asymmetry, testis and sperm size in Yellow Dung Flies. Funct Ecol. 2003;17:231-6. doi: 10.1046/j.1365-2435.2003.00723.x
    Howard DJ, Palumbi SR, Birge LM, Manier MK. Sperm and speciation. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: an evolutionary perspective. Amsterdam: Academic Press; 2009.
    Humphries S, Evans JP, Simmons LW. Sperm competition: linking form to function. BMC Evol Biol. 2008;8:319. doi: 10.1186/1471-2148-8-319
    Immler S, Calhim S, Birkhead TR. Increased postcopulatory sexual selection reduces the intra-male variation in sperm design. Evolution. 2008;62:1538-43. doi: 10.1111/j.1558-5646.2008.00393.x
    Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhim S, Birkhead TR. Resolving variation in the reproductive tradeoff between sperm size and number. P Natl Acad Sci USA. 2011;108:5325-30. doi: 10.1073/pnas.1009059108
    Jamieson BGM. Avian spermatozoa: structure and phylogeny. In: Jamieson BGM, editor. Reproductive biology and phylogeny of birds. Enfield, New Hampshire: Science Publisher; 2007.
    Jennings WB, Edwards SV. Speciational history of Australian grass finches (Poephila) inferred from thirty gene trees. Evolution. 2005;59:2033-47. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=10.1111/j.0014-3820.2005.tb01072.x
    Kleven O, Laskemoen T, Fossøy F, Robertson RJ, Lifjeld JT. Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution. 2007;62:494-9. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=10.1111/j.1558-5646.2007.00287.x
    Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT. Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution. 2009;63:2466-73. doi: 10.1111/j.1558-5646.2009.00725.x
    Landry C, Geyer LB, Arakaki Y, Uehara T, Palumbi SR. Recent speciation in the Indo-West Pacific: rapid evolution of gamete recognition and sperm morphology in cryptic species of sea urchin. Proc R Soc B. 2003;270:1839-47. doi: 10.1098/rspb.2003.2395
    Laskemoen T, Kleven O, Fossøy F, Lifjeld JT. Intraspecific variation in sperm lengthin two passerine species, the Bluethroat Luscinia svecica and the Willow Warbler Phylloscopus trochilus. Ornis Fennica. 2007;84:131-9.
    Laskemoen T, Kleven O, Fossøy F, Robertson RJ, Rudolfsen G, Lifjeld JT. Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallowTachycineta bicolor. Behav Ecol Sociobiol. 2010;64:1473-84. doi: 10.1007/s00265-010-0962-8
    Laskemoen T, Albrecht T, Bonisoli-Alquati A, Cepak J, Lope F, Hermosell IG, Johannessen LE, Kleven O, Marzal A, Mousseau TA, Møller AP, Robertson RJ, Rudolfsen G, Saino N, Vortman Y, Lifjeld JT. Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behav Ecol Sociobiol. 2013;67:301-9. doi: 10.1007/s00265-012-1450-0
    Lifjeld JT, Laskemoen T, Kleven O, Albrecht T, Robertson RJ. Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS One. 2010;5:e13456. doi: 10.1371/journal.pone.0013456
    Lifjeld JT, Hoenen A, Johannessen LE, Laskemoen T, Lopes RJ, Rodrigues P, Rowe M. The Azores bullfinch (Pyrrhula murina) has the same unusual and size-variable sperm morphology as the Eurasian bullfinch (Pyrrhula pyrrhula). Biol J Linn Soc. 2013;108:677-87. doi: 10.1111/j.1095-8312.2012.02040.x
    Lüpold S. Ejaculate quality and constraints in relation to sperm competition levels among eutherian mammals. Evolution. 2013;67:3052-60. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=10.1111/evo.12132
    Lüpold S, Calhim S, Immler S, Birkhead TR. Sperm morphology and sperm velocity in passerine birds. Proc R Soc B. 2009;276:1175-81. doi: 10.1098/rspb.2008.1645
    Lüpold S, Westneat DF, Birkhead TR. Geographical variation in sperm morphology in the red-winged blackbird (Agelaius phoeniceus). Evol Ecol. 2011;25:373-90. doi: 10.1007/s10682-010-9410-5
    Lüpold S, Manier MK, Berben KS, Smith KJ, Daley BD, Buckley SH, Belote JM, Pitnick S. How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr Biol. 2012;22:1667-72. doi: 10.1016/j.cub.2012.06.059
    Manier MK, Palumbi SR. Intraspecific divergence in sperm morphology of the green sea urchin, Strongylocentrotus droebachlensis: implications for selection in broadcast spawners. BMC Evol Biol. 2008;8:283. doi: 10.1186/1471-2148-8-283
    Manier MK, Belote JM, Berben KS, Lüpold S, Ala-Honkola O, Collins WF, Pitnick S. Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution. 2013a;67:2348-62. doi: 10.1111/evo.12117
    Manier MK, Lüpold S, Belote JM, Starmer WT, Berben KS, Ala-Honkola O, Collins WF, Pitnick S. Postcopulatory sexual selection generates speciation phenotypes in Drosophila. Curr Biol. 2013b;23:1853-62. doi: 10.1016/j.cub.2013.07.086
    Minoretti N, Baur B. Among- and within-population variation in sperm quality in the simultaneously hermaphroditic land snail Arianta arbustorum. Behav Ecol Sociobiol. 2006;60:270-80. doi: 10.1007/s00265-006-0165-5
    Møller AP. Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am Nat. 1991;137:882-906. doi: 10.1086/285199
    Mossman J, Slate J, Humphries S, Birkhead TR. Sperm morphology and velocity are genetically codetermined in the zebra finch. Evolution. 2009;63:2730-7. doi: 10.1111/j.1558-5646.2009.00753.x
    Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team. nlme: linear and nonlinear mixed effects models. R package version 3.1-118. 2014. http://CRAN.Rproject.org/package=nlme].
    Pitnick S, Miller GT, Schneider K, Markow TA. Ejaculate-female coevolution in Drosophila mojavensis. Proc R Soc B. 2003;270:1507-12. doi: 10.1098/rspb.2003.2382
    Pitnick S, Hosken DJ, Birkhead TR. Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: an evolutionary perspective. Amsterdam: Academic Press; 2009.
    Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: an evolutionary perspective. Amsterdam: Academic Press; 2009.
    Pizzari T, Worley K, Burke T, Froman DP. Sperm competition dynamics: ejaculate fertilising efficiency changes differentially with time. BMC Evol Biol. 2008;8:332-8.
    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013. http://www.Rproject.org/.
    Rollins LA, Svedin N, Pryke SR, Griffith SC. The role of the Ord Arid Intrusion in the historical and contemporary genetic division of long-tailed finch subspecies in northern Australia. Ecol Evol. 2012;2:1208-19. doi: 10.1002/ece3.259
    Rowe M, Pruett-Jones S. Sperm competition selects for sperm quantity and quality in the Australian Maluridae. PLoS One. 2011;6:e15720. doi: 10.1371/journal.pone.0015720
    Rowe M, Albrecht T, Cramer ERA, Johnsen A, Laskemoen T, Weir JT, Lifjeld JT. Postcopulatory sexual selection is associated with accelerated evolution of sperm morphology. Evolution. 2015;69:1044-52. doi: 10.1111/evo.12620
    Schmoll T, Kleven O. Sperm dimensions differ between two Coal Tit Periparus ater populations. J Ornithol. 2010;152:515-20. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=3ec2a219bca7012df4bf50b3f942059b
    Schodde R, Mason IJ. The directory of australian birds. Collingwood: CSIRO Publishing; 1999.
    Simmons LW, Fitzpatrick JL. Sperm wars and the evolution of male fertility. Reproduction. 2012;144:519-34. doi: 10.1530/REP-12-0285
    Simmons LW, Moore AJ. Evolutionary quantitative genetics of sperm. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: an evolutionary perspective. Amsterdam: Academic Press; 2009.
    Smith CC. Opposing effects of sperm viability and velocity on the outcome of sperm competition. Behav Ecol. 2012;23:820-6. doi: 10.1093/beheco/ars036
    Snook RR. Sperm in competition: not playing by the numbers. Trends Ecol Evol. 2005;20:46-53. doi: 10.1016/j.tree.2004.10.011
    Sokal RR, Rohlf FJ. Biometry: the principles and practice of statistics in biological research. San Francisco: Freeman; 1995.
    Stockley P, Gage MJG, Parker GA, Møller AP. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat. 1997;149:933-54. doi: 10.1086/286031
    Swanson WJ, Vacquier VD. The rapid evolution of reproductive proteins. Nat Rev Genet. 2002;3:137-44. http://cn.bing.com/academic/profile?id=8c67e08ff9386a418ce1da00e0a12a9d&encoded=0&v=paper_preview&mkt=zh-cn
    Töpfer T, Haring E, Birkhead TR, Lopes RJ, Severinghaus L, Martens J, Påckert M. A molecular phylogeny of bullfinches Pyrrhula Brisson, 1760 (Aves: Fringillidae). Mol Phylogenet Evol. 2011;58:271-82. doi: 10.1016/j.ympev.2010.10.015
    Tourmente M, Gomendio M, Roldan ERS. Sperm competition and the evolution of sperm design in mammals. BMC Evol Biol. 2011a;11:12. doi: 10.1186/1471-2148-11-12
    Tourmente M, Gomendio M, Roldan ERS. Mass-specific metabolic rate and sperm competition determine sperm size in marsupial mammals. PLoSone. 2011b;6:e21244. doi: 10.1371/journal.pone.0021244
    Van Rooij EP, Griffith SC. No evidence of assortative mating on the basis of putative ornamental traits in Long-tailed Finches Poephila acuticauda. Ibis. 2012;154:444-51. doi: 10.1111/j.1474-919X.2012.01233.x
    Varea-Sánchez M, Gómez Montoto L, Tourmente M, Roldan ERS. Postcopulatory sexual selection results in spermatozoa with more uniform head and flagellum sizes in rodents. PLoS One. 2014;9:e108148. doi: 10.1371/journal.pone.0108148
    Veen T, Borge T, Griffith SC, Saetre G-P, Bures S, Gustafsson L, Sheldon BC. Hybridization and adaptive mate choice in flycatchers. Nature. 2001;411:45-50. doi: 10.1038/35075000
    Wolfson A. The cloacal protuberance—a means for determining breeding condition in live male passerines. Bird Banding. 1952;23:159-65. doi: 10.2307/4510381
    Zann R. Variation in the songs of three species of Estrildine grassfinches. Emu. 1976;76:97-108. doi: 10.1071/MU9760097
    Zuur AF, Ieno EN, Walker NJ, Saveliev AA. Mixed effects models and extensions in ecology with R. New York: Springer; 2009.
    • Relative Articles
    • Supplements(0)
    • Cited By
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(2)  / Tables(2)

    Get Citation
    PDF
    XML

    Article Metrics

    Article views (204) PDF downloads(0) Cited by()
    Proportional views
    Supported by: Beijing Renhe Information Technology Co. Ltd   Technical support: info@rhhz.net

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return