Abstract
Fishes show a great diversity of mating systems and fertilization mechanisms. This diversity creates an enormous potential for sperm competition. Typically, monogamous species face a low risk of sperm competition and invest less into sperm, and thus show smaller relative testis mass compared to polygamous species with high sperm competition. In cichlids, sperm competition risk is very variable. In lacustrine East African cichlids, large sperm are interpreted as an adaptation to sperm competition, as in those species sperm length correlates with sperm swimming speed. The aim of the present study was to examine variation in sperm and testis traits of substrate breeding cichlids from West African river systems and its relationship to sperm competition. Therefore, sperm traits (total sperm size, flagellum-, midpiece-, and head size) and sperm number were related to the gonadosomatic index (GSI), an indicator of sperm competition, in eight species of two large informal tribes, the chromidotilapiines and the haplotilapiines. We found significant differences between species in all examined sperm traits, sperm number, and GSI with pronounced differences between chromidotilapiines and haplotilapiines. We used a generalized least-squares approach to control for non-independence of data. GSI was positively correlated with sperm number but negatively correlated with total sperm size (also negatively with the flagellum and head size but not significantly with midpiece size). Sperm number and sperm size were negatively correlated suggesting a trade-off between sperm size and quality. Our results suggest that large sperm can evolve in species with relatively low sperm expenditure and probably in absence of high sperm competition between males.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson MJ, Nyholt J, Dixson AE (2004) Sperm competition affects the structure of the mammalian vas deferens. J Zool 264:97–103. https://doi.org/10.1017/s095283690400559x
Bakker TCM, Hollmann M, Mehlis M, Zbinden M (2014) Functional variation of sperm morphology in sticklebacks. Behav Ecol Sociobiol 68:617–627. https://doi.org/10.1007/s00265-013-1676-5
Ball MA, Parker GA (1996) Sperm competition games: external fertilization and “adaptive” infertility. J Theor Biol 180:141–150 https://doi.org/10.1006/jtbi.1996.0090
Balshine S, Leach BJ, Neat F, Werner NY, Montgomerie R (2001) Sperm size of African cichlids in relation to sperm competition. Behav Ecol 12:726–731. https://doi.org/10.1093/beheco/12.6.726
Becker WA (1984) Manual of quantitative genetics. Academic Enterprises, Pullman
Bonanno VL, Schulte-Hostedde AI (2009) Sperm competition and ejaculate investment in red squirrels (Tamiasciurus hudsonicus). Behav Ecol Sociobiol 63:835–846. https://doi.org/10.1007/s00265-009-0718-5
Briskie JV, Montgomerie R, Birkhead TR (1997) The evolution of sperm size in birds. Evolution 51:937–945. https://doi.org/10.2307/2411167
Burness G, Casselman SJ, Schulte-Hostedde AI, Moyes CD, Montgomerie R (2004) Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behav Ecol Sociobiol 56:65–70. https://doi.org/10.1007/s00265-003-0752-7
Burness G, Moyes CD, Montgomerie R (2005) Motility, ATP levels and metabolic enzyme activity of sperm from bluegill (Lepomis macrochirus). Comp Biochem Physiol A Mol Integr Physiol 140:11–17. https://doi.org/10.1016/j.cbpb.2004.09.021
Burness G, Schulte-Hostedde AI, Montgomerie R (2008) Body condition influences sperm energetics in lake whitefish (Coregonus clupeaformis). Can J Fish Aquat Sci 65:615–620. https://doi.org/10.1139/f07-188
Byrne PG, Simmons LW, Roberts JD (2003) Sperm competition and the evolution of gamete morphology in frogs. Proc R Soc Lond B 270:2079–2086. https://doi.org/10.1098/rspb.2003.2433
de Vlaming V, Grossman GD, Chapman F (1982) On the use of the gonosomatic index. Comp Biochem Physiol 73:31–39. https://doi.org/10.1016/0300-9629(82)90088-3
Desjardins JK, Fitzpatrick JL, Stiver KA, Van der Kraak GJ, Balshine S (2008) Costs and benefits of polygyny in the cichlid Neolamprologus pulcher. Anim Behav 75:1771–1779. https://doi.org/10.1016/j.anbehav.2007.09.037
Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc Natl Acad Sci U S A 106:1128–1132. https://doi.org/10.1073/pnas.0809990106
Fitzpatrick JL, García-González F, Evans JP (2010) Linking sperm length and velocity: the importance of intramale variation. Biol Lett 6:797–799. https://doi.org/10.1098/rsbl.2010.0231
Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726. https://doi.org/10.1086/343873
Gage MJG (1994) Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc R Soc Lond B 258:247–254. https://doi.org/10.1098/rspb.1994.0169
Gage MJG, Morrow EH (2003) Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Curr Biol 13:754–757. https://doi.org/10.1016/s0960-9822(03)00282-3
Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47. https://doi.org/10.1016/j.cub.2003.12.028
Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc R Soc Lond B 243:181–185. https://doi.org/10.1098/rspb.1991.0029
Gomendio M, Roldan ERS (2008) Implications of diversity in sperm size and function for sperm competition and fertility. Int J Dev Biol 52:439–447. https://doi.org/10.1387/ijdb.082595mg
Grafen A (1989) The phylogenetic regression. Philos Trans R Soc Lond B 326:119–157. https://doi.org/10.1098/rstb.1989.0106
Harvey PH, Purvis A (1991) Comparative methods for explaining adaptations. Nature 351:619–624. https://doi.org/10.1038/351619a0
Hellmann JK, O'Connor CM, Ligocki IY, Farmer TM, Arnold TJ, Reddon AR, Garvy KA, Marsh-Rollo SE, Balshine S, Hamilton IM (2015) Evidence for alternative male morphs in a Tanganyikan cichlid fish. J Zool 296:116–123. https://doi.org/10.1111/jzo.12222
Hilke L (2011) Spermienallokation im intersexuellen Kontext beim Dreistachligen Stichling (Gasterosteus aculeatus). Diploma thesis, University ofBonn
Humphries S, Evans JP, Simmons LW (2008) Sperm competition: linking form to function. BMC Evol Biol 8:319. https://doi.org/10.1186/1471-2148-8-319
Immler S, Birkhead TR (2007) Sperm competition and sperm midpiece size: no consistent pattern in passerine birds. Proc R Soc Lond B 274:561–568. https://doi.org/10.1098/rspb.2006.3752
Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhim S, Birkhead TR (2011) Resolving variation in the reproductive tradeoff between sperm size and number. Proc Natl Acad Sci U S A 108:5325–5330. https://doi.org/10.1073/pnas.1009059108
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64. https://doi.org/10.1017/s0006323199005423
Kokko H, Jennions MD, Brooks R (2006) Unifying and testing models of sexual selection. In: Annual Review of Ecology Evolution and Systematics, vol 37. Annu Rev Ecol Evol S 37:43-66. doi:https://doi.org/10.1146/annurev.ecolsys.37.091305.110259
Lamboj A (2004) Die Cichliden des westlichen Afrikas. Birgit Schmettkamp Verlag, Bornheim
LaMunyon CW, Ward S (1999) Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proc R Soc Lond B 266:263–267 https://doi.org/10.1098/rspb.1999.0631
Langen K, Bakker TCM, Baldauf SA, Shrestha J, Thünken T (2017) Effects of ageing and inbreeding on the reproductive traits in a cichlid fish I: the male perspective. Biol J Linn Soc 120:752-761. https://doi.org/10.1093/biolinnean/blw002
Laskemoen T, Kleven O, Fossoy F, Lifjeld JT (2007) Intraspecific variation in sperm length in two passerine species, the Bluethroat Luscinia svecica and the Willow Warbler Phylloscopus trochilus. Ornis Fenn 84:131–139
Laskemoen T, Albrecht T, Bonisoli-Alquati A, Cepak J, de Lope F, Hermosell IG, Johannessen LE, Kleven O, Marzal A, Mousseau TA, Møller AP, Robertson RJ, Rudolfsen G, Saino N, Vortman Y, Lifjeld JT (2013) Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behav Ecol Sociobiol 67:301–309. https://doi.org/10.1007/s00265-012-1450-0
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121https://doi.org/10.2307/4087240
Lüpold S, Calhim S, Immler S, Birkhead TR (2009) Sperm morphology and sperm velocity in passerine birds. Proc R Soc Lond B 276:1175–1181. https://doi.org/10.1098/rspb.2008.1645
Malo AF, Gomendio M, Garde J, Lang-Lenton B, Soler AJ, Roldan ERS (2006) Sperm design and sperm function. Biol Lett 2:246–249. https://doi.org/10.1098/rsbl.2006.0449
Martin E, Taborsky M (1997) Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success. Behav Ecol Sociobiol 41:311–319 https://doi.org/10.1007/s002650050391
Martinez ML, Mullin V, Schulte-Hostedde A (2015) Variation in sperm morphometry of the African cyprinid Barbus neumayeri (Neumayer’s barb). Can J Zool 93:259–266. https://doi.org/10.1139/cjz-2014-0196
Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667. https://doi.org/10.1086/286013
Møller AP, Briskie JV (1995) Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav Ecol Sociobiol 36:357–365. https://doi.org/10.1007/bf00167797
Montgomerie R, Fitzpatrick JL (2009) Testis size, sperm size and sperm competition. In: Jamieson BGM (ed) Reproductive biology and phylogeny of fishes (agnathans and bony fishes) Volume 8B. Science Publishers, Enfield, pp 1–53
Neff BD, Fu P, Gross MR (2003) Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus). Behav Ecol 14:634–641https://doi.org/10.1093/beheco/arg032
Nunn CL (2011) The comparative approach in evolutionary anthropology and biology. The University of Chicago Press, Chicago
Orme CDL, Freckleton RP, Thomas GH, Petzholdt T, Fritz SA, Isaak NJB (2013) Caper: comparative analyses of phylogenetics and evolution in R. Methods Ecol Evol 3:145–151
Ota K, Heg D, Hori M, Kohda M (2010) Sperm phenotypic plasticity in a cichlid: a territorial male’s counterstrategy to spawning takeover. Behav Ecol 21:1293–1300. https://doi.org/10.1093/beheco/arq146
Pagel M (1997) Inferring evolutionary processes from phylogenies. Zool Scr 26:331–348. https://doi.org/10.1111/j.1463-6409.1997.tb00423.x
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884. https://doi.org/10.1038/44766
Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567 https://doi.org/10.1111/j.1469-185X.1970.tb01176.x
Parker GA (1982) Why are there so many tiny sperm - sperm competition and the maintenance of two sexes. J Theor Biol 96:281–294. https://doi.org/10.1016/0022-5193(82)90225-9
Parker GA (1990a) Sperm competition games - raffles and roles. Proc R Soc Lond B 242:120–126 https://doi.org/10.1098/rspb.1990.0114
Parker GA (1990b) Sperm competition games - sneaks and extra-pair copulations. Proc R Soc Lond B 242:127–133 https://doi.org/10.1098/rspb.1990.0115
Parker GA (1993) Sperm competition games - sperm size and sperm number under adult control. Proc R Soc Lond B 253:245–254. https://doi.org/10.1098/rspb.1993.0110
Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 3–54
Parker GA (2016) The evolution of expenditure on testes. J Zool 298:3–19. https://doi.org/10.1111/jzo.12297
Parker GA, Begon ME (1993) Sperm competition games: sperm size and number under gametic control. Proc R Soc Lond B 253:255–262. https://doi.org/10.1098/rspb.1993.0111
Parker GA, Smith VGF, Baker RR (1972) Origin and evolution of gamete dimorphism and male-female phenomenon. J Theor Biol 36:529. https://doi.org/10.1016/0022-5193(72)90007-0
Petersen CW, Warner RR (1998) Sperm competition in fishes. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, Oxford, pp 435–463
Pitnick S (1996) Investment in testes and the cost of making long sperm in Drosophila. Am Nat 148:57–80. https://doi.org/10.1086/285911
Pitnick S, Spicer GS, Markow TA (1995) How long is a giant sperm. Nature 375:109–109. https://doi.org/10.1038/375109a0
Pitnick S, Hosken DJ, Birkhead TR (2009) Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective, vol 1. Academic Press, Oxford, pp 69–149
R Development Core Team (2009) R: a language and environment for statistical computing. R foundation for Statistical Computing, Vienna
Sato T, Hirose M, Taborsky M, Kimura S (2004) Size-dependent male alternative reproductive tactics in the shell-brooding cichlid fish Lamprologus callipterus in Lake Tanganyika. Ethology 110:49–62 https://doi.org/10.1046/j.1439-0310.2003.00944.x
Schulte-Hostedde AI, Millar JS (2004) Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behav Ecol Sociobiol 55:272–277. https://doi.org/10.1007/s00265-003-0707-z
Schütz D, Pachler G, Ripmeester E, Goffinet O, Taborsky M (2010) Reproductive investment of giants and dwarfs: specialized tactics in a cichlid fish with alternative male morphs. Funct Ecol 24:131–140. https://doi.org/10.1111/j.1365-2435.2009.01605.x
Schwarzer J, Lamboj A, Langen K, Misof B, Schliewen UK (2015) Phylogeny and age of chromidotilapiine cichlids (Teleostei: Cichlidae). Hydrobiologia 748:185–199. https://doi.org/10.1007/s10750-014-1918-1
Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton
Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53. https://doi.org/10.1016/j.tree.2004.10.011
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman and Company, New York
Stockley P, Gage MJG, Parker GA, Møller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149:933–954. https://doi.org/10.1086/286031
Taborsky M (1994) Sneakers, satellites, and helpers - parasitic and cooperative behavior in fish reproduction. Adv Study Behav 23:1–100 https://doi.org/10.1016/S0065-3454(08)60351-4
Taborsky M (2008) Alternative reproductive tactics in fish. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics, vol 1. Cambridge University Press, Cambridge, pp 251–299
Thünken T, Bakker TCM, Kullmann H (2007) Extraordinarily long sperm in the socially monogamous cichlid fish Pelvicachromis taeniatus. Naturwissenschaften 94:489–491. https://doi.org/10.1007/s00114-007-0217-3
Tomkins JL, Simmons LW (2002) Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim Behav 63:1009–1016. https://doi.org/10.1006/anbe.2001.1994
Vladić TV, Jarvi T (2001) Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism. Proc R Soc Lond B 268:2375–2381. https://doi.org/10.1098/rspb.2001.1768
Vladić TV, Afzelius BA, Bronnikov GE (2002) Sperm quality as reflected through morphology in salmon alternative life histories. Biol Reprod 66:98–105. https://doi.org/10.1095/biolreprod66.1.98
Walter B, Trillmich F (1994) Female agression and male peace-keeping in a cichlid harem - conflict between and within sexes in Lamprologus ocellatus. Behav Ecol Sociobiol 34:105–112. https://doi.org/10.1007/bf00164181
Acknowledgments
We thank the Bakker research group for discussion. We thank Julia Schwarzer, Museum Alexander Koenig Bonn, for help with the phylogeny and for providing the phylogenetic tree in Fig. 1. We are grateful to Dagmar Wenzel for help and support with the SEM. We acknowledge the help of Jujina Shrestha and Etienne Nkusi on experiments concerning sperm activation in P. taeniatus. We thank Chris Petersen, Sven Thatje, and anonymous referees for useful comments on the manuscript.
Funding
This work was supported by the Deutsche Forschungsgemeinschaft (DFG) (BA 2885/2-3).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Matthias Waltert
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 28 kb)
Rights and permissions
About this article
Cite this article
Langen, K., Thünken, T., Klemm, J. et al. Sperm size is negatively related to relative testis size in West African riverine cichlid fishes. Sci Nat 106, 30 (2019). https://doi.org/10.1007/s00114-019-1622-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-019-1622-0