Abstract
Polygynous males increase their reproductive success by fertilizing as many females as possible. However, this strategy can lead to costs for the males. This study focused on an atypical wolf spider that lives in webs, Aglaoctenus lagotis. Previous studies report polyandrous females, but little is known about the mating strategy of males and its potential associated costs. Our goals were to determine the potential polygyny and the changes in sexual behaviour, body condition and physiology of males throughout successive matings. Males were expected to mate with multiple females; males’ body condition was expected to decrease and male mating performance, including sperm transfer, was expected to decrease over successive matings. Males were exposed to successive virgin females every 3 days until the male did not court, was cannibalized or died of natural causes. Agreeing with our predictions, males were capable of multiple matings, showing an average of 5 ± 2 matings (range 3–11). Their mating performance decreased in successive matings and, although no changes were found in the behavioural patterns during the courtship over successive matings, the number of palpal insertions decreased. Unexpectedly, overall body condition did not decrease and males did not deplete their sperm supply. We found that 44% of the males were victims of sexual cannibalism after their third mating. The females that attacked or cannibalized males had less sperm stored in their spermathecae than those that did not. We discuss hypotheses that may clarify this scenario and the role of the cryptic female choice mechanism.
This is a preview of subscription content, log in via an institution to check access.
References
Aisenberg A, Costa FG (2005) Females mated without sperm transfer maintain high sexual receptivity level in the wolf spider Schizocosa malitiosa. Ethology 111:545–558. https://doi.org/10.1111/j.1439-0310.2005.01077.x
Aisenberg A, Peretti AV (2011) Sexual dimorphism in immune response, fat reserves and muscle mass in a sex role reversed spider. Zoology 114:272–275
Aisenberg A, Viera C, Costa FG (2007) Daring females, devoted males and reversed sexual size dimorphism in the sand-dwelling spider Allocosa brasiliensis (Araneae, Lycosidae). Behav Ecol Sociobiol 62:29–35. https://doi.org/10.1007/s00265-007-0435-xDO
Alavi Y, Elgar MA, Jones TM (2016) Male mating success and the effect of mating history on ejaculate traits in a facultatively parthenogenic insect (Extatosoma tiaratum). Ethology 122:523–530. https://doi.org/10.1111/eth.12497
Anderson AG, Hebets EA (2017) Increased insertion number leads to increased sperm transfer and fertilization success in a nursery web spider. Anim Behav 132:121–127. https://doi.org/10.1016/j.anbehav.2017.08.007
Anderson AG, Hebets EA, Bickner BM, Watts JC (2018) Males mate with multiple females to increase offspring numbers in a nursery web spider. Behav Ecol 29(4):918–924. https://doi.org/10.1093/beheco/ary054
Barbosa F (2011) Copulation duration in the soldier fly: the roles of cryptic male choice and sperm competition risk. Behav Ecol 22:1332–1336. https://doi.org/10.1093/beheco/arr137
Barry KL, Holwell G, Herberstein ME (2008) Female praying mantids use sexual cannibalism as a foraging strategy to increase fecundity. Behav Ecol 19:710–715. https://doi.org/10.1093/beheco/arm156
Baruffaldi L, Costa FG (2010) Changes in male sexual responses from silk cues of females at different reproductive states in the wolf spider Schizocosa malitiosa. J Ethol 28:75–85. https://doi.org/10.1007/s10164-009-0158-8
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823
Berger-Tal R, Lubin Y (2011) High male mate search costs and a female-biased sex ratio shape the male mating strategy in a desert spider. Anim Behav 82:853–859. https://doi.org/10.1016/j.anbehav.2011.07.021
Blumstein DT, Evans CS, Daniel JC (2000) JWatcher. Online at http://galliform.psy.mq.edu.au/jwatcher/. Accessed Mar 2017
Bucher E (1974) Observaciones ecológicas sobre artrópodos del bosque chaqueño de Tucumán. Revista de Facultad de Ciencias Exactas Físicas y Naturales de Córdoba (NS). Biología 1:35–122
Ceballos L, Jones TM, Elgar MA (2015) Patterns of sperm transfer in the golden orb-weaver Nephila edulis. Ethol 121:617–624. https://doi.org/10.1111/eth.12375
Costa FG (1979) Análisis de la cópula y de la actividad postcopulatoria de Lycosa malitiosa Tullgren (Araneae: Lycosidae). Rev Brasil Biol 39:361–376
Damiens D, Boivin G (2005) Male reproductive strategy in Trichogramma evanescens: sperm production and allocation to females. Physiol Entomol 30(3):241–247. https://doi.org/10.1111/j.1365-3032.2005.00453.x
Delignette-Muller ML, Dutang LC (2015) fitdistrplus: an R package for fitting distributions. J Stat Softw 64:1–34
DeVito J, Meik JM, Gerson MM, Formanowicz DR Jr (2004) Physiological tolerances of three sympatric riparian wolf spiders (Araneae: Lycosidae) correspond with microhabitat distributions. Can J Zool 82:1119–1125
Elgar MA, Crespi BJ (1992) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, New York
Elgar MA, Nash DR (1988) Sexual cannibalism in the garden spider Araneus diadematus. Anim Behav 36:1511–1517. https://doi.org/10.1016/S0003-3472(88)80221-5
Elgar MA, Schneider JM (2004) The evolutionary significance of sexual cannibalism. Adv Stud Behav 34:135–163. https://doi.org/10.1016/S0065-3454(04)34004-0
Elgar MA, Schneider JM, Herberstein ME (2000) Female control of paternity in the sexually cannibalistic spider. Proc R Soc London Ser B 267(1460):2439–2443
Engqvist L, Sauer KP (2003) Determinants of sperm transfer in the scorpionfly Panorpa cognata: male variation, female condition and copulation duration. J Evol Biol 16:1196–1204. https://doi.org/10.1046/j.1420-9101.2003.00613.x
Fernández-Montraveta C, Cuadrado M (2013) Hogna radiata males do not deplete their sperm in a single mating. J Arachnol 41:102–107. https://doi.org/10.1636/Hi12-72.1
Fernández-Montraveta C, Ortega J (1990) Some aspects of the reproductive behavior of Lycosa tarentula fasciiventris (Araneae, Lycosidae). J Arachnol 18:257–262. https://doi.org/10.1007/s10164-009-0158-8
Foelix R (2011) Biology of spiders, 3rd edn. Oxford University Press, Inc., Cary
Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielse A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:2,233–2,249. https://doi.org/10.1080/10556788.2011.597854
Fujisaki K (1981) Studies on the mating system of the winter cherry bug, Acanthocoris sordidus Thunberg (Heteroptera: Coreidae) II. Harem defence polygyny. Res Popul Ecol 23:262–279. https://doi.org/10.1007/BF02515630DO
García-Díaz V, Aisenberg A, Peretti AV (2015) Communication during copulation in the sex-role reversed wolf spider Allocosa brasiliensis: female shakes for soliciting new ejaculations? Behav Process 116:62–68. https://doi.org/10.1016/j.beproc.2015.05.005
Gaskett AC, Herberstein ME, Downes BJ, Elgar MA (2004) Changes in male mate choice in a sexually cannibalistic orb-web spider (Araneae: Araneidae). Behaviour 141:1197–1210
González M (2015) Aspectos reproductivos de Aglaoctenus lagotis: estudio interpoblacional de una araña lobo sedentaria de gran variabilidad fenotípica. Tesis de doctorado de Ciencias Biológicas, FCEFyN, Universidad Nacional de Córdoba, Argentina
González M (2018) Are multiple copulations harmful? Damage to male pedipalps in the funnel-web wolf spider Aglaoctenus lagotis (Araneae: Lycosidae). J Arachnol 46:162–164. https://doi.org/10.1636/JoA-S-17-017.1
González M, Peretti AV, Viera C, Costa FG (2013) Differences in sexual behavior of two distant populations of the funnel-web wolf spider Aglaoctenus lagotis. J Ethol 31:175–184. https://doi.org/10.1007/s10164-013-0365-1DO
González M, Costa FG, Peretti AV (2014) Strong phenological differences between two populations of a Neotropical funnel-web wolf spider. J Nat Hist 48:2183–2197. https://doi.org/10.1080/00222933.2014.908974
González M, Peretti AV, Costa FG (2015) Reproductive isolation between two populations of Aglaoctenus lagotis, a funnel-web wolf spider. Biol J Linn Soc 114:646–658. https://doi.org/10.1111/bij.12448
González M, Costa FG, Peretti AV (2019) Different levels of polyandry in two populations of the funnel-web wolf spider Aglaoctenus lagotis from South America. https://doi.org/10.1007/s10164-019-00606-5
Grafe TU (1997) Costs and benefits of mate choice in the lek-breeding reed frog, Hyperolius marmoratus. Anim Behav 53:1103–1117. https://doi.org/10.1006/anbe.1996.0427
Gwynne DT (1987) Sex-biased predation and the risky mate-locating behaviour of male tick-tock cicadas (Homoptera, Cicadidae). Anim Behav 35:571–576. https://doi.org/10.1016/S0003-3472(87)80283-X
Heer L (2013) Male and female reproductive strategies and multiple paternity in the polygynandrous Alpine Accentor Prunella collaris. J Ornithol 154:251–264. https://doi.org/10.1007/s10336-012-0891-6DO
Herberstein ME, Schneider JM, Elgar MA (2002) Costs of courtship and mating in a sexually cannibalistic orb-web spider: female strategies and their consequences for males. Behav Ecol Sociobiol 51:440–446. https://doi.org/10.1007/s00265-002-0460-8
Herberstein ME, Schneider JM, Harmer AMT, Gaskett AC, Robinson K, Shaddick K, Soetkamp D,Wilson PD, Pekar S, Elgar MA (2011) Sperm storage and copulation duration in a sexually cannibalistic spider. J Ethol 29(1):9–15. https://doi.org/10.1007/s10164-010-0213-5
Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S, Hothorn MT (2016) Package ‘multcomp’. Simultaneous inference in general parametric models. Project for Statistical Computing, Vienna
Hughes L, Siew-Woon Chang B, Wagner D, Pierce NE (2000) Effects of mating history on ejaculate size, fecundity, longevity, and copulation duration in the ant-tended lycaenid butterfly Jalmenus evagoras. Behav Ecol Sociobiol 47:119–128. https://doi.org/10.1007/s002650050002DO
Jiao X, Chen Z, Wu J, Du H, Liu F, Chen J, Li D (2011) Male remating and female fitness in the wolf spider Pardosa astrigera: the role of male mating history. Behav Ecol Sociobiol 65:325–332. https://doi.org/10.1007/s00265-010-1049-2DO
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108. https://doi.org/10.1016/j.tree.2003.10.013
Jones TM (2001) A potential cost of monandry in the lekking sandfly Lutzomyia longipalpis. J Insect Behav 14:385–397. https://doi.org/10.1023/A:1011127514317DO
Jones TM, McNamara KB, Colvin P, Featherston R, Elgar MA (2006) Mating frequency, fecundity and fertilization success in the hide beetle, Dermestes maculatus. J Insect Behav 19:357–371. https://doi.org/10.1007/s10905-006-9032-5DO
Kasumovic MM, Bruce MJ, Herberstein ME, Andrade MCB (2007) Risky mate search and mate preference in the golden orb-web spider (Nephila plu- mipes). Behav Ecol 18:189–195. https://doi.org/10.1093/beheco/arl072
Kotiaho JS, Simmons LW (2003) Longevity cost of reproduction for males but no longevity cost of mating or courtship for females in the male-dimorphic dung beetle Onthophagus binodis. J Insect Physiol 49:817–822. https://doi.org/10.1016/S0022-1910(03)00117-3
Lange R, Gruber B, Henle K, Sarre DS, Hoehna M (2013) Mating system and intrapatch mobility delay inbreeding in fragmented populations of a gecko. Behav Ecol 24:1260–1270. https://doi.org/10.1093/beheco/art060
Lauwers K, Van Dyck H (2006) The cost of mating with a non-virgin male in a monandrous butterfly: experimental evidence from the speckled wood Pararge aegeria. Behav Ecol Sociobiol 60:69–76. https://doi.org/10.1007/s00265-005-0142-4DO
Masumoto T (1991) Males’ visits to females’ webs and female mating receptivity in the spider, Agelena limbata (Araneae: Agelenidae). J Ethol 9:1–7
Modanu M, Michalik P, Andrade MCB (2013) Mating system does not predict permanent sperm depletion in black widow spiders. Evol Dev 15(3):205–212. https://doi.org/10.1111/ede.12034
Molina Y, Christenson T (2008) Effects of mating experience on subsequent reproductive behaviour and sperm release in the spider Nesticodes rufipes. Anim Behav 76(4):1327–1334
Mowles SL, Jepson NM (2015) Physiological costs of repetitive courtship displays in cockroaches handicap locomotor performance. PLoS One 10:e0143664. https://doi.org/10.1371/journal.pone.0143664
Moya-Laraño J, Pascual J, Wise DH (2003) Mating patterns in late maturing female Mediterranean tarantulas may reflect the costs and benefits of sexual cannibalism. Anim Behav 66:469–476. https://doi.org/10.1006/anbe.2003.2262
Norton S, Uetz WG (2005) Mating frequency in Schizocosa ocreata (Hentz) wolf spider: evidence for a mating system with female monandry and male polygyny. J Arachnol 33:16–24. https://doi.org/10.1636/S02-72
Papke MJ, Riechert SE, Schulz S (2001) An airborne female pheromone associated with male attraction and courtship in a desert spider. Anim Behav 61:877–886. https://doi.org/10.1006/anbe.2000.1675
Paukku S, Kotiaho JS (2005) Cost of reproduction in Callosobruchus maculatus: effects of mating on male longevity and the effect of male mating status on female longevity. J Insect Physiol 51:1220–1226. https://doi.org/10.1016/j.jinsphys.2005.06.012
Pérez-Miles F, Postiglioni R, Montes de Oca L, Baruffaldi L, Costa FG (2007) Mating system in the tarantula spider Eupalestrus weijenberghi (Thorell, 1894): evidences of monandry and polygyny. Zoology 110:253–260. https://doi.org/10.1016/j.zool.2007.01.001
Perez-Staples D, Aluja M (2006) Sperm allocation and cost of mating in a tropical tephritid fruit fly. J Insect Physiol 52:839–845. https://doi.org/10.1016/j.jinsphys.2006.05.007
Pérez-Staples D, Aluja M, Macías-Ordóñez R, Sivinski J (2008) Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua. Behav Ecol Sociobiol 62(8):1333–1340. https://doi.org/10.1007/s00265-008-0561-0DO
Persons MH, Uetz GW (2005) Sexual cannibalism and mate choice decisions in wolf spiders: influences of male size and secondary sexual characters. Anim Behav 69:83–94. https://doi.org/10.1016/j.anbehav.2003.12.030
Prenter J, MacNeil C, Elwood RW (2006) Sexual cannibalism and mate choice. Anim Behav 71:481–490. https://doi.org/10.1016/j.anbehav.2005.05.011
Rasband W (2014) ImageJ 1.48v. National Institute of Health, USA. http://imagej.nih.gov/ij. Java 1.6.0 20(64-bit). Access April 2019
R Core Team (2017) R: A language and environment for statistical computing. https://www.R-project.org/. Access April 2019
Roggenbuck H, Pekár S, Schneider JM (2011) Sexual cannibalism in the European garden spider Araneus diadematus: the roles of female hunger and mate size dimorphism. Anim Behav 81:749–755. https://doi.org/10.1016/j.anbehav.2011.01.005
Rovner JS (1971) Mechanims controlling copulatory behavior in wolf spiders (Araneae, Lycosidae). Psyche 78:150–165
Rovner JS, Wright EE (1975) Copulation in spider: experimental evidence for fatigue effects and bilateral control of palpal insertions. Anim Behav 23:233–236. https://doi.org/10.1016/0003-3472(75)90069-X
Rubolini D, Galeotti P, Pupin F, Sacchi R, Nardi PA, Fasola M (2007) Repeated matings and sperm depletion in the freshwater crayfish Austropotamobius italicus. Freshw Biol 52:1898–1906. https://doi.org/10.1111/j.1365-2427.2007.01814.x
Rypstra AL, Wieg C, Walker SE, Persons MH (2003) Mutual mate assessment in wolf spiders: differences in the cues used by males and females. Ethology 109:315–325. https://doi.org/10.1046/j.1439-0310.2003.00874.x
Schäfer MA, Uhl G (2005) Sequential mate encounters: female but not male body size influences female remating behavior. Behav Ecol 16(2):461–466. https://doi.org/10.1093/beheco/ari013
Schneider JM, Lesmono K (2009) Courtship raises male fertilization success through post-mating sexual selection in a spider. Proc R Soc B Biol Sci 276:3105–3111. https://doi.org/10.1098/rspb.2009.0694
Schneider J, Michalik P (2011) One-shot genitalia are not an evolutionary dead end—regained male polygamy in a sperm limited spider species. BMC Evol Biol 11:197. https://doi.org/10.1186/1471-2148-11-197
Shamble PS, Wilgers DJ, Swoboda KA, Hebets EA (2009) Courtship effort is a better predictor of mating success than ornamentation for male wolf spiders. Behav Ecol 20:1242–1251. https://doi.org/10.1093/beheco/arp116
Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton
Simmons LW (2002) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton
Singer F, Riechert ES (1995) Mating system and mating success of the desert spider Agelenopsis aperta. Behav Ecol Sociobiol 36:313–322. https://doi.org/10.1007/BF00167792DO
Snow LSE, Andrade MCB (2004) Pattern of sperm transfer in redback spiders: implications for sperm competition and male sacrifice. Behav Ecol 15:785–792. https://doi.org/10.1093/beheco/arh080
Sordi S (1996) Ecologia de populaçoes da aranha Porrimosa lagotis (Lycosidae) nas reservas Mata de Santa Genebra, Campinas (SP) e Serra do Japi, Jundai (SP). PhD Thesis, Universidade Estadual de Campinas, Sao Paulo, Brasil
Toscano-Gadea CA, Costa FG (2016) Description of the sexual behavior of the Neotropical wolf spider Pavocosa gallopavo (Araneae:Lycosidae), with comments on sexual cannibalism. J Arachnol 44:412–416. https://doi.org/10.1636/J15-75.1
Uhl G (1994) Genital morphology and sperm storage in Pholcus phalangioides (Fuesslin, 1775) (Pholcidae; Araneae). Acta Zool (Stockholm) 75(1):1–12. https://doi.org/10.1111/j.1463-6395.1994.tb00957.x
Vrech D, Olivero PA, Mattoni CI, Peretti AV (2018) From storage to delivery: sperm volume and number of spermatozoa inside storage organs and ejaculates in males of Timogenes elegans (Scorpiones: Bothriuridae). J Arachnol 46:231–239. https://doi.org/10.1636/JoA-S-16-097.1
Wedell N, Ritchie MG (2004) Male age, mating status and nuptial gift quality in a bushcricket. Anim Behav 67:1059–1065. https://doi.org/10.1016/j.anbehav.2003.10.007
Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm limited females. Trends Ecol Evol 17:313–320. https://doi.org/10.1016/S0169-5347(02)02533-8
Welke KW, Schneider JM (2012) Sexual cannibalism benefits offspring survival. Anim Behav 83:201–207. https://doi.org/10.1016/j.anbehav.2011.10.027
Wilder SM, Rypstra AL (2007) Male control of copulation duration in a wolf spider (Araneae, Lycosidae). Behaviour 144:471–484. https://doi.org/10.1163/156853907780756012
Willisch SC, Biebach I, Koller U, Bucher T, Marreros N, Degiorgis RPM, Keller FL, Neuhaus P (2012) Male reproductive pattern in a polygynous ungulate with a slow life-history: the role of age, social status and alternative mating tactics. Evol Ecol 26:187–206. https://doi.org/10.1007/s10682-011-9486-6DO
World Spider Catalog (2018) World Spider Catalog. Natural History Museum Bern, online at http://wsc.nmbe.ch, version 18.0. Accessed 10 June 2018
Acknowledgements
We want to thank Franco Cargnelutti, Matias Izquierdo, Mariela Oviedo-Diego, Javier Rial, Luna Silvetti and Cecilia Naval for their help in collecting the spiders. We are also very grateful to Mariela Oviedo-Diego and Germán González for the statistical support. Franco Cargnelutti gave us valuable technical assistance with sperm count. Marc Weed revised the language. Finally, we thank the anonymous reviewers who have contributed to the improvement of the manuscript substantially.
Funding
This study was supported by the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), SECYT UNC and Fondo para la Investigación Científica y Tecnológica (FONCYT) of Argentina.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
A. lagotis mating, showing the male over the female (in the typical lycosid mating position). The female body shakings that occur during mating, and the moment of the dismount can be observed (MP4 20.6 mb)
A. lagotis mating, showing the moment of cannibalism occurrence (MP4 33.2 mb)
Rights and permissions
About this article
Cite this article
Abregú, D.A., Peretti, A.V. & González, M. Male performance and associated costs in successive sexual encounters in a polygynous web wolf spider. acta ethol 22, 175–186 (2019). https://doi.org/10.1007/s10211-019-00323-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10211-019-00323-9