Last-male sperm precedence breaks down when females mate with three males
1994; Royal Society; Volume: 257; Issue: 1350 Linguagem: Inglês
10.1098/rspb.1994.0127
ISSN1471-2954
Autores Tópico(s)Plant and animal studies
ResumoRestricted accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Zeh Jeanne A. and Zeh David W. 1994Last-male sperm precedence breaks down when females mate with three malesProc. R. Soc. Lond. B.257287–292http://doi.org/10.1098/rspb.1994.0127SectionRestricted accessArticleLast-male sperm precedence breaks down when females mate with three males Jeanne A. Zeh Google Scholar Find this author on PubMed Search for more papers by this author and David W. Zeh Google Scholar Find this author on PubMed Search for more papers by this author Jeanne A. Zeh Google Scholar Find this author on PubMed and David W. Zeh Google Scholar Find this author on PubMed Published:22 September 1994https://doi.org/10.1098/rspb.1994.0127AbstractFemales of many species commonly mate with several males, yet our knowledge of sperm precedence patterns is based almost exclusively on laboratory experiments in which females were mated to only two males. In both birds and insects, these investigations have generally shown strong mating order effects, usually with the second male to mate siring most of the offspring. In the harlequin beetle-riding pseudoscorpion, single-locus minisatellite DNA profiling has recently revealed extensive multiple paternity within the broods of field-inseminated females. Here, we report the findings of a sperm precedence experiment in which we investigated this unusual absence of mating order effects. By allowing females to mate with only two males, we were able experimentally to induce the pattern of strong last-male sperm precedence typical of other two-male mating studies. By contrast, females mated to three males produced broods exhibiting the same highly mixed paternity detected in this species in nature. The elimination of mating order constraints on sperm utilization when females mate with several males suggests that the opportunity for post-copulatory sexual selection may be much greater in nature than is evident from two-male mating experiments.FootnotesThis text was harvested from a scanned image of the original document using optical character recognition (OCR) software. As such, it may contain errors. Please contact the Royal Society if you find an error you would like to see corrected. Mathematical notations produced through Infty OCR. 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Moura R, Oliveira I, Vasconcellos‐Neto J, Gonzaga M and Goymann W (2020) "Where ignorance is bliss, 'tis folly to be wise": Indiscriminate male care in a neotropical spider, Ethology, 10.1111/eth.13112, 127:3, (223-230), Online publication date: 1-Mar-2021. Johansson F, Berger D, Höglund J, Meyer-Lucht Y, Rödin-Mörch P, Sniegula S and Watts P (2020) High variation in last male sperm precedence and genital morphology in the emerald damselfly, Lestes sponsa, Biological Journal of the Linnean Society, 10.1093/biolinnean/blaa055, 130:3, (497-506), Online publication date: 26-Jun-2020. Rodrigues L, Figueiredo A, Van Leeuwen T, Olivieri I, Magalhães S and Sheldon B (2020) Costs and benefits of multiple mating in a species with first‐male sperm precedence, Journal of Animal Ecology, 10.1111/1365-2656.13171, 89:4, (1045-1054), Online publication date: 1-Apr-2020. LeGrice R, Tezanos‐Pinto G, de Villemereuil P, Holwell G and Painting C (2019) Directional selection on body size but no apparent survival cost to being large in wild New Zealand giraffe weevils, Evolution, 10.1111/evo.13698, 73:4, (762-776), Online publication date: 1-Apr-2019. Turnell B, Shaw K and Reeve H (2018) Modeling strategic sperm allocation: Tailoring the predictions to the species, Evolution, 10.1111/evo.13423, 72:3, (414-425), Online publication date: 1-Mar-2018. Lymbery R, Kennington W and Evans J (2018) Multivariate Sexual Selection on Ejaculate Traits under Sperm Competition, The American Naturalist, 10.1086/697447, 192:1, (94-104), Online publication date: 1-Jul-2018. Fortin M, Debenest C, Souty-Grosset C and Richard F (2018) Males prefer virgin females, even if parasitized, in the terrestrial isopod Armadillidium vulgare , Ecology and Evolution, 10.1002/ece3.3858, 8:6, (3341-3353), Online publication date: 1-Mar-2018. Laturney M, van Eijk R and Billeter J (2018) Last male sperm precedence is modulated by female remating rate in Drosophila melanogaster , Evolution Letters, 10.1002/evl3.50, 2:3, (180-189), Online publication date: 1-Jun-2018. Parker D, Zaborowska J, Ritchie M and Vahed K (2017) Paternity analysis of wild-caught females shows that sperm package size and placement influence fertilization success in the bushcricket Pholidoptera griseoaptera , Molecular Ecology, 10.1111/mec.14089, 26:11, (3050-3061), Online publication date: 1-Jun-2017. Hook K (2017) Female remating decisions and a shorter inter-mating interval diminish last-male sperm precedence, Behavioral Ecology and Sociobiology, 10.1007/s00265-017-2350-0, 71:8, Online publication date: 1-Aug-2017. Karageorge K and Wilson R (2017) An integrative mating system assessment of a nonmodel, economically important Pacific rockfish ( Sebastes melanops ) reveals nonterritorial polygamy and conservation implications for a large species flock , Ecology and Evolution, 10.1002/ece3.3579, 7:24, (11277-11291), Online publication date: 1-Dec-2017. Droge-Young E, Belote J, Perez G and Pitnick S (2016) Resolving mechanisms of short-term competitive fertilization success in the red flour beetle, Journal of Insect Physiology, 10.1016/j.jinsphys.2016.06.003, 93-94, (1-10), Online publication date: 1-Oct-2016. Bocedi G and Reid J (2014) Evolution of female multiple mating: A quantitative model of the "sexually selected sperm" hypothesis, Evolution, 10.1111/evo.12550, 69:1, (39-58), Online publication date: 1-Jan-2015. Rovelli V, Randi E, Davoli F, Macale D, Bologna M and Vignoli L (2015) She gets many and she chooses the best: polygynandry in Salamandrina perspicillata (Amphibia: Salamandridae) , Biological Journal of the Linnean Society, 10.1111/bij.12613, 116:3, (671-683), Online publication date: 1-Nov-2015. West R (2014) The evolution of large brain size in birds is related to social, not genetic, monogamy, Biological Journal of the Linnean Society, 10.1111/bij.12193, 111:3, (668-678), Online publication date: 1-Mar-2014. Friesen C, Kerns A and Mason R (2014) Factors influencing paternity in multiply mated female red-sided garter snakes and the persistent use of sperm stored over winter, Behavioral Ecology and Sociobiology, 10.1007/s00265-014-1749-0, 68:9, (1419-1430), Online publication date: 1-Sep-2014. Zimmer S, Schneider J and Herberstein M (2014) Can males detect the strength of sperm competition and presence of genital plugs during mate choice?, Behavioral Ecology, 10.1093/beheco/aru045, 25:4, (716-722), Online publication date: 1-Jul-2014. Walter D and Proctor H (2013) Sex and Celibacy Mites: Ecology, Evolution & Behaviour, 10.1007/978-94-007-7164-2_5, (105-159), . Novo M, Fernández R, Granado-Yela C, Gutiérrez López M and Díaz Cosín D (2013) Does the order of copulation matter? Experimental paternity analyses in the earthworm Hormogaster elisae (Annelida: Hormogastridae), Pedobiologia, 10.1016/j.pedobi.2013.01.002, 56:2, (97-104), Online publication date: 1-Mar-2013. Billeter J, Jagadeesh S, Stepek N, Azanchi R and Levine J (2012) Drosophila melanogaster females change mating behaviour and offspring production based on social context, Proceedings of the Royal Society B: Biological Sciences, 279:1737, (2417-2425), Online publication date: 22-Jun-2012. Elgee K, Ramnarine I and Pitcher T (2011) Multiple paternity, reproductive skew and correlates of male reproductive success in a wild population of the Trinidadian guppy, Ecology of Freshwater Fish, 10.1111/j.1600-0633.2011.00528.x, 21:1, (109-118), Online publication date: 1-Jan-2012. Demont M, Martin O and Bussière L (2011) Wild yellow dung fly females may not select sperm based on dung pat microclimate but could nevertheless benefit from polyandry, Evolutionary Ecology, 10.1007/s10682-011-9519-1, 26:3, (715-731), Online publication date: 1-May-2012. Leftwich P, Edward D, Alphey L, Gage M and Chapman T (2012) Variation in adult sex ratio alters the association between courtship, mating frequency and paternity in the lek-forming fruitfly Ceratitis capitata, Journal of Evolutionary Biology, 10.1111/j.1420-9101.2012.02556.x, 25:9, (1732-1740), Online publication date: 1-Sep-2012. Soper D, Delph L and Lively C (2012) Multiple paternity in the freshwater snail, Potamopyrgus antipodarum , Ecology and Evolution, 10.1002/ece3.408, 2:12, (3179-3185), Online publication date: 1-Dec-2012. Engqvist L (2012) A GENERAL DESCRIPTION OF ADDITIVE AND NONADDITIVE ELEMENTS OF SPERM COMPETITIVENESS AND THEIR RELATION TO MALE FERTILIZATION SUCCESS, Evolution, 10.1111/evo.12024, (no-no), Online publication date: 1-Dec-2012. Jellen B and Aldridge R (2011) Paternity Patterns Reproductive Biology and Phylogeny of Snakes, 10.1201/b10879-17, (619-644), Online publication date: 15-Apr-2011. Bonilla M, Zeh D, White A and Zeh J (2011) Discriminating Males and Unpredictable Females: Males Bias Sperm Allocation in Favor of Virgin Females, Ethology, 10.1111/j.1439-0310.2011.01928.x, 117:8, (740-748), Online publication date: 1-Aug-2011. GAREFALAKI M, TRIANTAFYLLIDIS A, ABATZOPOULOS T and STAIKOU A (2010) The outcome of sperm competition is affected by behavioural and anatomical reproductive traits in a simultaneously hermaphroditic land snail, Journal of Evolutionary Biology, 10.1111/j.1420-9101.2010.01964.x, 23:5, (966-976), Online publication date: 1-May-2010. House C, Hunt J and Moore A (2007) Sperm competition, alternative mating tactics and context-dependent fertilization success in the burying beetle, Nicrophorus vespilloides, Proceedings of the Royal Society B: Biological Sciences, 274:1615, (1309-1315), Online publication date: 22-May-2007.Bjork A, Starmer W, Higginson D, Rhodes C and Pitnick S (2007) Complex interactions with females and rival males limit the evolution of sperm offence and defence, Proceedings of the Royal Society B: Biological Sciences, 274:1619, (1779-1788), Online publication date: 22-Jul-2007. SIMMONS L, BEVERIDGE M and KENNINGTON W (2007) Polyandry in the wild: temporal changes in female mating frequency and sperm competition intensity in natural populations of the tettigoniid Requena verticalis , Molecular Ecology, 10.1111/j.1365-294X.2007.03528.x, 16:21, (4613-4623), Online publication date: 1-Nov-2007. Knox T and Scott M (2005) Size, operational sex ratio, and mate-guarding success of the carrion beetle, Necrophila americana, Behavioral Ecology, 10.1093/beheco/arj004, 17:1, (88-96), Online publication date: 1-Jan-2006. ENGQVIST L and REINHOLD K (2006) Theoretical influence of female mating status and remating propensity on male sperm allocation patterns, Journal of Evolutionary Biology, 10.1111/j.1420-9101.2006.01134.x, 19:5, (1448-1458), Online publication date: 1-Sep-2006. Blyth J and Gilburn A (2005) The effect of an inversion system and the time interval between matings on postcopulatory sexual selection in the seaweed fly, Coelopa frigida, Heredity, 10.1038/sj.hdy.6800713, 95:2, (174-178), Online publication date: 1-Aug-2005. Dunn D, Sumner J and Goulson D (2005) The benefits of multiple mating to female seaweed flies, Coelopa frigida (Diptera: Coelpidae), Behavioral Ecology and Sociobiology, 10.1007/s00265-005-0922-x, 58:2, (128-135), Online publication date: 1-Jun-2005. Morrow E, Stewart A and Rice W (2005) PATTERNS OF SPERM PRECEDENCE ARE NOT AFFECTED BY FEMALE MATING HISTORY IN DROSOPHILA MELANOGASTER, Evolution, 10.1554/05-238.1, 59:12, (2608), . Morrow E, Stewart A and Rice W (2005) PATTERNS OF SPERM PRECEDENCE ARE NOT AFFECTED BY FEMALE MATING HISTORY IN DROSOPHILA MELANOGASTER, Evolution, 10.1111/j.0014-3820.2005.tb00973.x, 59:12, (2608-2615), Online publication date: 1-Dec-2005. Kamimura Y (2004) Last-male paternity of Euborellia plebeja, an earwig with elongated genitalia and sperm-removal behavior, Journal of Ethology, 10.1007/s10164-004-0125-3, 23:1, (35-41), Online publication date: 1-Jan-2005. Hockham L, Graves J and Ritchie M (2004) Sperm competition and the level of polyandry in a bushcricket with large nuptial gifts, Behavioral Ecology and Sociobiology, 10.1007/s00265-004-0838-x, 57:2, (149-154), Online publication date: 1-Dec-2004. Simmons L, Beveridge M and Krauss S (2004) Genetic analysis of parentage within experimental populations of a male dimorphic beetle, Onthophagus taurus, using amplified fragment length polymorphism, Behavioral Ecology and Sociobiology, 10.1007/s00265-004-0843-0, 57:2, (164-173), Online publication date: 1-Dec-2004. Bernasconi G, Paschke M and Schmid B (2003) Diversity effects in reproductive biology, Oikos, 10.1034/j.1600-0706.2003.12598.x, 102:1, (217-220), Online publication date: 1-Jul-2003. Liewlaksaneeyanawin C, Ritland K, Ritland C and El-Kassaby Y (2003) Experimental analysis of the mating system of the white pine weevil, Pissodes strobi (Peck) (Coleoptera: Curculionidae) , Canadian Journal of Zoology, 10.1139/z03-026, 81:3, (424-429), Online publication date: 1-Mar-2003. Roderick G, de Mendoza L, Dively G and Follett P Sperm Precedence in Colorado Potato Beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae): Temporal Variation Assessed by Neutral Markers, Annals of the Entomological Society of America, 10.1603/0013-8746(2003)096[0631:SPICPB]2.0.CO;2, 96:5, (631-636) Drnevich J (2003) Number of mating males and mating interval affect last-male sperm precedence in Tenebrio molitor L., Animal Behaviour, 10.1006/anbe.2003.2219, 66:2, (349-357), Online publication date: 1-Aug-2003. Franck P, Solignac M, Vautrin D, Cornuet J, Koeniger G and Koeniger N (2002) Sperm competition and last-male precedence in the honeybee, Animal Behaviour, 10.1006/anbe.2002.3078, 64:3, (503-509), Online publication date: 1-Sep-2002. Vermette R and Fairbairn D (2002) HOW WELL DO MATING FREQUENCY AND DURATION PREDICT PATERNITY SUCCESS IN THE POLYGYNANDROUS WATER STRIDER AQUARIUS REMIGIS?, Evolution, 10.1111/j.0014-3820.2002.tb00195.x, 56:9, (1808-1820), Online publication date: 1-Sep-2002. Kraaijeveld-Smit F, Ward S, Temple-Smith P and Paetkau D (2002) Factors influencing paternity success in Antechinus agilis: last-male sperm precedence, timing of mating and genetic compatibility, Journal of Evolutionary Biology, 10.1046/j.1420-9101.2002.00367.x, 15:1, (100-107), Online publication date: 1-Jan-2002. Vermette R and Fairbairn D (2002) HOW WELL DO MATING FREQUENCY AND DURATION PREDICT PATERNITY SUCCESS IN THE POLYGYNANDROUS WATER STRIDER AQUARIUS REMIGIS?, Evolution, 10.1554/0014-3820(2002)056[1808:HWDMFA]2.0.CO;2, 56:9, (1808), . Paterson I, Partridge V and Buckland-Nicks J (2001) Multiple Paternity in Littorina obtusata (Gastropoda, Littorinidae) Revealed by Microsatellite Analyses , The Biological Bulletin, 10.2307/1543508, 200:3, (261-267), Online publication date: 1-Jun-2001. Campbell V and Fairbairn D (2001) Prolonged copulation and the internal dynamics of sperm transfer in the water strider Aquarius remigis , Canadian Journal of Zoology, 10.1139/z01-148, 79:10, (1801-1812), Online publication date: 1-Oct-2001. Simmons L (2001) The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses, Journal of Evolutionary Biology, 10.1046/j.1420-9101.2001.00309.x, 14:4, (585-594) Zeh J and Zeh D (2001) Spontaneous abortion depresses female sexual receptivity in a viviparous arthropod, Animal Behaviour, 10.1006/anbe.2001.1790, 62:3, (427-433), Online publication date: 1-Sep-2001. Garner T, Brinkmann H, Gerlach G, Meyer A, Ward P, SpOrri M and Hosken D (2000) Polymorphic DNA microsatellites identified in the yellow dung fly (Scathophaga stercoraria), Molecular Ecology, 10.1046/j.1365-294X.2000.105328.x, 9:12, (2207-2209), Online publication date: 1-Dec-2000. Eady P, Wilson N and Jackson M (2000) COPULATING WITH MULTIPLE MATES ENHANCES FEMALE FECUNDITY BUT NOT EGG-TO-ADULT SURVIVAL IN THE BRUCHID BEETLE CALLOSOBRUCHUS MACULATUS, Evolution, 10.1554/0014-3820(2000)054[2161:CWMMEF]2.0.CO;2, 54:6, (2161), . Eady P, Wilson N and Jackson M (2000) COPULATING WITH MULTIPLE MATES ENHANCES FEMALE FECUNDITY BUT NOT EGG-TO-ADULT SURVIVAL IN THE BRUCHID BEETLE CALLOSOBRUCHUS MACULATUS, Evolution, 10.1111/j.0014-3820.2000.tb01259.x, 54:6, (2161-2165), Online publication date: 1-Dec-2000. Harvey I and Parker G (2000) 'Sloppy' sperm mixing and intraspecific variation in sperm precedence ( P 2 ) patterns , Proceedings of the Royal Society of London. Series B: Biological Sciences, 10.1098/rspb.2000.1317, 267:1461, (2537-2542), Online publication date: 22-Dec-2000. Haubruge E, Arnaud L, Mignon J and Gage M (1999) Fertilization by proxy: rival sperm removal and translocation in a beetle, Proceedings of the Royal Society of London. Series B: Biological Sciences, 10.1098/rspb.1999.0761, 266:1424, (1183-1187), Online publication date: 7-Jun-1999. Newcomer S, Zeh J and Zeh D (1999) Genetic benefits enhance the reproductive success of polyandrous females, Proceedings of the National Academy of Sciences, 10.1073/pnas.96.18.10236, 96:18, (10236-10241), Online publication date: 31-Aug-1999. Arnqvist G and Danielsson I (2017) COPULATORY BEHAVIOR, GENITAL MORPHOLOGY, AND MALE FERTILIZATION SUCCESS IN WATER STRIDERS, Evolution, 10.1111/j.1558-5646.1999.tb05340.x, 53:1, (147-156), Online publication date: 1-Feb-1999. Curach N and Sunnucks P (1999) Molecular anatomy of an onychophoran: compartmentalized sperm storage and heterogeneous paternity, Molecular Ecology, 10.1046/j.1365-294x.1999.00698.x, 8:9, (1375-1385), Online publication date: 1-Sep-1999. WATSON P (1998) Multi-male mating and female choice increase offspring growth in the spiderNeriene litigiosa(Linyphiidae), Animal Behaviour, 10.1006/anbe.1997.0593, 55:2, (387-403), Online publication date: 1-Feb-1998. Simmons L and Siva-Jothy M (1998) Sperm Competition in Insects: Mechanisms and the Potential for Selection Sperm Competition and Sexual Selection, 10.1016/B978-012100543-6/50035-0, (341-434), . Elgar M (1998) Sperm Competition and Sexual Selection in Spiders and Other Arachnids Sperm Competition and Sexual Selection, 10.1016/B978-012100543-6/50034-9, (307-339), . UHL G (1998) Mating behaviour in the cellar spider,Pholcus phalangioides, indicates sperm mixing, Animal Behaviour, 10.1006/anbe.1998.0854, 56:5, (1155-1159), Online publication date: 1-Nov-1998. Zeh J, Newcomer S and Zeh D (1998) Polyandrous females discriminate against previous mates, Proceedings of the National Academy of Sciences, 10.1073/pnas.95.23.13732, 95:23, (13732-13736), Online publication date: 10-Nov-1998. Scott M and Williams S (1998) Molecular measures of insect fitness Molecular Approaches to Ecology and Evolution, 10.1007/978-3-0348-8948-3_3, (55-69), . Calos J and Sakaluk S (1998) Paternity of offspring in multiply–mated, female crickets: the effect of nuptial food gifts and the advantage of mating first, Proceedings of the Royal Society of London. Series B: Biological Sciences, 10.1098/rspb.1998.0558, 265:1411, (2191-2195), Online publication date: 22-Nov-1998. Zeh D, Zeh J and Bermingham E (1997) Polyandrous, sperm-storing females: carriers of male genotypes through episodes of adverse selection, Proceedings of the Royal Society of London. Series B: Biological Sciences, 264:1378, (119-125), Online publication date: 22-Jan-1997. Radwan J (1997) Sperm precedence in the bulb mite, Rhizoglyphus robini : context-dependent variation , Ethology Ecology & Evolution, 10.1080/08927014.1997.9522879, 9:4, (373-383), Online publication date: 1-Oct-1997. Greenfield M (1997) Sexual Selection and the Evolution of Advertisement Signals Communication, 10.1007/978-1-4899-1745-4_6, (145-177), . Cooper G, Miller P and Holland P (1997) Molecular genetic analysis of sperm competition in the damselfly Ischnura elegans (Vander Linden), Proceedings of the Royal Society of London. Series B: Biological Sciences, 263:1375, (1343-1349), Online publication date: 22-Oct-1996.Boomsma J and Ratnieks F (1997) Paternity in eusocial Hymenoptera, Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 351:1342, (947-975), Online publication date: 29-Jul-1996. HAASE M and BAUR B (1995) Variation in spermathecal morphology and storage of spermatozoa in the simultaneously hermaphroditic land snail Arianta arbustorum (Gastropoda: Pulmonata: Stylommatophora) , Invertebrate Reproduction & Development, 10.1080/07924259.1995.9672461, 28:1, (33-41), Online publication date: 1-Jul-1995. This Issue22 September 1994Volume 257Issue 1350 Article InformationDOI:https://doi.org/10.1098/rspb.1994.0127Published by:Royal SocietyPrint ISSN:0962-8452Online ISSN:1471-2954History: Manuscript received23/05/1994Manuscript accepted10/06/1994Published online01/01/1997Published in print22/09/1994 License:Scanned images copyright © 2017, Royal Society Citations and impact Large datasets are available through Proceedings B's partnership with Dryad
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