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Sperm precedence is the tendency of a female who has bred with multiple males to produce the offspring of those males in unequal proportions. It thus only occurs in species breeding through sexual reproduction and with gametes of different sizes (anisogamy), which the majority of sexually reproducing species have.

Not all sexually reproducing species with anisogamy exhibit multiple mating by males with each reproductive female, so it has not been identified in all sexually reproducing species. Nevertheless, anisogamy leads to sperm competition and sperm selection, aspects of sexual selection, so sperm precedence is an important factor in the occurrence of postcopulatory sexual selection[1] in species with such behaviour.

Sperm competition

Main article: Sperm competition

Why sperm competition?

Sperm competition occurs in sexually reproducing species that have unequally sized gametes, that is they exhibit anisogamy. But why should gametes be of different sizes?

There have been a number of suggestions of why this occurs in many species, but one relates to the advantage that a sex producing smaller microgamates (sperm) has in attempts at fertilisation of macrogametes (ova). Because macrogametes are much more costly to produce the sex producing them cannot keep up with the number of microgametes produced by the other sex.

Thus if selection starts on the gametes of one sex in a sexually reproducing species with equally sized gametes (isogamy), selection towards smaller gametes is likely to be successful.[2] This cannot continue indefinitely, because microgametes must carry the genetic material of one sex, and must contain organelles to make them motile towards macrogames and to enable them to fuse with a macrogamete to form a zygote.

What is sperm competition?

In anisogamous species, because one sex produces many more microgametes than the other does macrogametes, microgametes (sperm) compete with each other for successful fertisation of each ova.[a] This occurs irrespective of the mating behaviour of the males producing the sperm.

However where male-female mating behaviour involves competition by males for access to females, then sperm competition can become more complex.[3]

When does sperm precedence occur?

Sperm precedence requires the same conditions as sperm competition and sperm selection. But they[b] cannot be identified in all species where these have been identified, because it requires example species where:

  • Females normally mate with multiple males.
  • It is ethically sound to investigate the progress of sperm from multiple males in fertilising each female.
  • It is ethically sound to reproduce this investigation across replicates of females.

It is thus not surpring that sperm precedence or sperm selection have been identified in less groups of organisms, typically invertebrates, than sperm competition. (See Table 6.2[3]: 128  for examples of taxa where sperm competition has been identified.) Nevertheless, if these conditions can be satisfied, then sperm precedence can be investigated.

Examples of sperm precedence

Sperm precedence has been identified in diverse groups of animals where females mate with multiple males. Examples are given in the table below. It is not surprising that many are found in insects, the most diverse group of Arthropoda and far more diverse (that is, including far more species) than the whole of vertebrates, the group containing mammals. Another group where examples are found are arachnids, including many spiders.

Birds are a group of vertebrates where some species are bred domestically, and the example given here is a species, the Japanese quail, studied to improve breeding success. The discovery of sperm precdence was not the main focus.[4]

The only mammalian example is the house mouse because it has been bred for experimental work (the laboratory mouse) and thus can satisfy ethical requirements for lab work on mammals.[5]

Sperm precedence in animals
Group[c] Species Common name
Insects Panorpa germanica L. German scorpionfly[6]
Anthidium manicatum European wool carder bee[7]
Tenebrio molitor L. Yellow mealworm beetle[8]
Callosobruchus maculatus Cowpea seed beetle[9]
Eriopis connexa (Germar) Ladybird beetle[10]
Harmonia axyridis (Pallas) Harlequin, Asian or multicoloured Asian ladybird beetle[11]
Drosophila melanogaster Fruit fly[12]
Apis mellifera Western honey bee[13]
Ephestia kuehniella Mediterranean flour moth[14]
Dryomyza anilis Fly[d][15]
Scathophaga stercoraria L. Yellow dung fly[16]
Tribolium castaneum (Herbst) Red flour beetle[17]
Arachnids Misumena vatia Goldenrod crab spider or flower crab spider[18]
Pisaura mirabilis Predatory spider, cunning spider or bridal gift spider[19]
Birds Coturnix japonica Japanese quail or cotornix quail[4]
Mammals Mus musculus House mouse[e][5]

Types of sperm precedence

The most frequently found types of sperm precedence are temporal, that is relating to the order in which a male mates with a female in a sequence of matings. If the first male to mate is likely to have an advantage, then sperm precedence is described as first male precedence. If the last male to mate is likely to have an advantage, then sperm precedence is described as last male precedence.

Other types of sperm precedence have been suggested. Sperm precedence can favor the male whose sperm are the most motile,[4] or the male whose sperm were delivered closest to the female’s ova.

The species where sperm precedence has been identified in the table shown in Examples of sperm precedence above give indication of where the different types of sperm precedence occur.

Species exhibiting different types of sperm precedence

Many insects exhibit last male precedence.[20] This includes Anthidium manicatum the European wool carder bee, although the authors of the research on this species also write: “Or at least ‘late’ male precedence”.[7]: 211  This suggests some change in advantage in the sperm precedence of later males.

Of those insect species given in the table above the two ladybird beetle species Eriopis connexa[10] and Harmonia axyridis[11] are the exceptions. Eriopis connexa is included because it is a species where males and females mate multiple times with each other and the reference provided was a search for sperm precedence.[10] However, no consistent trend for sperm precedence was found. Harmonia axyridis, in contrast to most other insect species, exhibits first male precedence.

The two spider species given, also invertbrates, but part of Arachnida rather than Arthropoda the group to which insects belong, both exhibit first male precedence.[18][19]

The house mouse example is unusual. The only reason it can be included is that it has been bred for laboratory work and thus satisfies ethical standards. Researchers in the study given suggested that last male precedence could be found in breeding among certain haplotypes distinct from the wildtype.[5]

Mechanisms for sperm precedence

As already mentioned, many insect species exhibit last male precedence.[20] But one of the insect species considered here exhibits firat male precedence.

Either of these phenomena may be a consequence of the reproductive anatomy of insects. Female insects (and females of some other groups) have spermathecae, organs that can receive and store sperm from males following mating. Thus, the existence of spermathecae means that sperm do not travel directly to ova during reproduction and sperm competition between early- or late-mating males may be controlled by female behaviour.[21]

Mating plugs formed within the female reproductive tract can have a role in sperm storage, but also in female remating, and thus support first male precedence.[22]

Mating of females with multiple males can enable sperm displacement. An early example of this was identified in dung flies, supporting last male precedence.[23] Later models confirmed how this form of mating behaviour including sperm displacement could result in last male precendence.[24]

What this observation of behaviour combined with modelling could not do was confirm the movement of the copulating male’s ejaculate through the female’s reproductive tract. A technique to monitor this added a final piece of evidence. Different males were labelled with different radioisotopes, allowing their sperm to be tracked in the female reproductive tract.[16]

The use of radioisotopes confirmed last male precedence in the yellow dung fly, but through an indirect rather than direct process of sperm displacement. Male yellow dung flies copulate into an organ of the female reproductive system called the bursa copulatrix. Sperm received there are transferred into the female’s spermathacae. Each female has three spermathacae, where sperm can be stored for some time before being used for fertilization. As a consequence the bursa copulatrix may be a location for sperm displacement, but sperm dispacement in the spermathacae is needed to result in sperm precedence during multiple mating.[25]

Notes

  1. ^ The term ova is used here rather than egg because egg has multiple usages.
  2. ^ Sperm competition and sperm selection.
  3. ^ Not all taxonmic groups are equivalent.
  4. ^ No other details of common name.
  5. ^ The house mouse bred for laboratory research.

References

  1. ^ Lipshutz, Sara E.; Torneo, Samuel J.; Rosvall, Kimberly A. (2023). “How Female-Female Competition Affects Male-Male Competition: Insights into Postcopulatory Sexual Selection from Socially Polyandrous Species”. The American Naturalist. 201 (3): 460–471. doi:10.1086/722799. PMID 36848510.
  2. ^ Parker, G A; Baker, R R; Smith, V G F (1972). “The origin and evolution of gamete dimorphism and the male-female phenomenon”. Journal of Theoretical Biology. 36 (3): 529–553. doi:10.1016/0022-5193(72)90007-0. PMID 5080448.
  3. ^ a b Birkhead, Timothy R; Parker, Geoffrey A (1997). “Chapter 6: Sperm Competition and Mating Systems”. In Krebs, J R; Davies, N B (eds.). Behavioural Ecology: An Evolutionary Approach (4th ed.). Oxford, UK: Blackwell Scientific. pp. 121–145. ISBN 9780865427310.
  4. ^ a b c Matsuzaki, Mei; Hirohashi, Noritaka; Tsudzuki, Masaoki; Haqani, Mohammad Ibrahim; Maeda, Teruo; Mizushima, Shusei; Sasanami, Tomohiro (2021). “Longer and faster sperm exhibit better fertilization success in Japanese quail”. Poultry Science. 100 (4) 100980. doi:10.1016/j.psj.2021.01.003. PMC 7905478. PMID 33610899.
  5. ^ a b c Sutter, Andreas; Lindholm, Anna K. (2016). “Meiotic drive changes sperm precedence patterns in house mice: Potential for male alternative mating tactics?”. BMC Evolutionary Biology. 16 (1) 133. doi:10.1186/s12862-016-0710-4. PMC 4915163. PMID 27328665.
  6. ^ Kock, Dagmar; Sauer, Klaus P. (2007). “High variation in sperm precedence and last male advantage in the scorpionfly Panorpa germanica L. (Mecoptera, Panorpidae): Possible causes and consequences”. Journal of Insect Physiology. 53 (11): 1145–1150. doi:10.1016/j.jinsphys.2007.06.002. PMID 17632122.
  7. ^ a b Lampert, Kathrin P.; Pasternak, Vanessa; Brand, Philipp; Tollrian, Ralph; Leese, Florian; Eltz, Thomas (2014). “‘Late’ male sperm precedence in polyandrous wool-carder bees and the evolution of male resource defence in Hymenoptera”. Animal Behaviour. 90: 211–217. doi:10.1016/j.anbehav.2014.01.034.
  8. ^ Drnevich, Jenny M. (2003). “Number of mating males and mating interval affect last-male sperm precedence in Tenebrio molitor L”. Animal Behaviour. 66 (2): 349–357. doi:10.1006/anbe.2003.2219.
  9. ^ Eady, Paul E.; Rugman-Jones, Paul; Brown, Denise V. (2004). “Prior oviposition, female receptivity and last-male sperm precedence in the cosmopolitan pest Callosobruchus maculatus (Coleoptera: Bruchidae)”. Animal Behaviour. 67 (3): 559–565. doi:10.1016/j.anbehav.2003.07.003.
  10. ^ a b c Silva, Alessandra C.G.; Silva-Torres, Christian S.A.; Nascimento, Deividy V.; Torres, Jorge B. (2021). “Sexual maturity, lack of partner choice and sperm precedence in the promiscuous ladybird beetle Eriopis connexa (Germar): Who is my father?”. Behavioural Processes. 192 104500. doi:10.1016/j.beproc.2021.104500. PMID 34509563.
  11. ^ a b Awad, Mona; Piálek, Lubomír; Krejčí, Alena; Laugier, Guillaume; Nedvěd, Oldřich (2017). “Paternity following multiple mating in ladybird Harmonia axyridis”. Biocontrol. 62 (3): 297–307. doi:10.1007/s10526-017-9806-z. hdl:11104/0272006.
  12. ^ Laturney, Meghan (2018). “Last male sperm precedence is modulated by female remating rate in Drosophila melanogaster”. Evolution Letters. 2 (3): 180–189. doi:10.1002/evl3.50. PMC 6121866. PMID 30283675.
  13. ^ Franck, Pierre; Solignac, Michel; Vautrin, Dominique; Cornuet, Jean-Marie; Koeniger, Gudrun; Koeniger, Nikolaus (2002). “Sperm competition and last-male precedence in the honeybee”. Animal Behaviour. 64 (3): 503–509. doi:10.1006/anbe.2002.3078.
  14. ^ Xu, Jin; Wang, Qiao (2010). “Thiotepa, a reliable marker for sperm precedence measurement in a polyandrous moth”. Journal of Insect Physiology. 56 (1): 102–106. doi:10.1016/j.jinsphys.2009.09.009. PMID 19799908.
  15. ^ Otronen, Merja (1997). “Variation in sperm precedence during mating in male flies, Dryomyza anilis”. Animal Behaviour. 53 (6): 1233–1240. doi:10.1006/anbe.1996.0425. PMID 9236019.
  16. ^ a b Simmons, L.W.; Parker, G. A.; Stockley, P. (1999). “Sperm Displacement in the Yellow Dung Fly, Scatophaga stercoraria: An Investigation of Male and Female Processes”. American Naturalist. 153 (3): 302–314. doi:10.1086/303171. PMID 29585969.
  17. ^ Haubruge, Eric; Arnaud, Ludovic; Mignon, Jacques (1997). “The Impact of Sperm Precedence in Malathion Resistance Transmission in Populations of the Red Flour Beetle Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae)”. Journal of Stored Product Research. 33 (2): 143–146. doi:10.1016/S0022-474X(96)00045-8. hdl:2268/26120.
  18. ^ a b Morse, Douglass H. (2010). “Male mate choice and female response in relation to mating status and time since mating”. Behavioral Ecology. 21 (2): 250–256. doi:10.1093/beheco/arp183.
  19. ^ a b Matzke, Magdalena; Toft, Søren; Bechsgaard, Jesper; Pold Vilstrup, Astrid; Uhl, Gabriele; Künzel, Sven; Tuni, Cristina; Bilde, Trine (2022). “Sperm competition intensity affects sperm precedence patterns in a polyandrous gift-giving spider”. Molecular Ecology. 31 (8): 2435–2452. doi:10.1111/mec.16405. PMID 35178803.
  20. ^ a b Parker, G. A. (1970). “Sperm competition and its evolutionary consequences in the insects”. Biol. Rev. 45 (4): 525–567. doi:10.1111/j.1469-185X.1970.tb01176.x.
  21. ^ Ward, Paul I. (2000). “Cryptic Female Choice in the Yellow Dung Fly Scathophaga Stercoraria (L.)”. Evolution. 54 (5): 1680–1686. doi:10.1111/j.0014-3820.2000.tb00712.x. PMID 11108595.
  22. ^ Bretman, Amanda; Lawniczak, Mara K.N.; Boone, James; Chapman, Tracey (2010). “A mating plug protein reduces early female remating in Drosophila melanogaster”. Journal of Insect Physiology. 56 (1): 107–113. doi:10.1016/j.jinsphys.2009.09.010. PMID 19800888.
  23. ^ Parker, G. A. (1970). “Sperm competition and its evolutionary effect on copula duration in the dung flie Scatophago stercoraria L.”. Journal of Insect Physiology. 16: 1301–1328. doi:10.1016/0022-1910(70)90131-9.
  24. ^ Parker, G. A.; Simmons, L. W.; Kirk, H (1990). “Analysing sperm competition data: simple models for predicting mechanisms”. Behav. Ecol. Sociobiol. 27: 55–65. doi:10.1007/BF00183314.
  25. ^ Parker, G. A.; Simmons, L. W. (2000). “Optimal copula duration in yellow dung flies: ejaculatory duct dimensions and size-dependent sperm displacement”. Evolution. 54 (3): 924–935. doi:10.1111/j.0014-3820.2000.tb00092.x. PMID 10937265.