Eunuchs: The Role of Apyrene Sperm in Lepidoptera?

Silberglied, Robert E.; Shepherd, Julian; Dickinson, Janis L.

doi:10.1086/284200

Cited by 205 publications

(193 citation statements)

References 44 publications

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“…However, the increased production of oligopyrene sperm, both in number and proportion of sperm produced, when in the presence of large numbers of potential rivals strongly suggests these sperm play a role in sperm competition, as proposed for other non-fertilizing sperm (e.g. Silberglied et al 1984). Similar results have been reported for the armyworm Pseudaletia seperata.…”

Section: Discussionsupporting

confidence: 77%

“…The`cheap ¢ller' hypothesis suggests that the highly motile apyrene sperm, which persist in the spermathecae along with the eupyrene sperm, deceive the sensory system of the female's spermathecae, delaying receptivity (Silberglied et al 1984;Cook & Gage 1995). Moreover, because the apyrene sperm of lepidopterans are smaller and simpler than eupyrene sperm, they are likely to be cheaper to produce (Gage & Cook 1994;Cook & Gage 1995).…”

Section: Discussionmentioning

confidence: 99%

“…If oligopyrene sperm play a role in sperm competition, as has been proposed for other non-fertilizing sperm (e.g. Silberglied et al 1984;Cook & Gage 1995), the quantity produced may be a¡ected by varying sperm competition risk. However, because non-fertilizing sperm morphs, and possibly functions, di¡er appreciably across taxa, the in£uence of sperm competition on sperm production may also vary.…”

Section: Introductionmentioning

confidence: 99%

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Snail sperm production characteristics vary with sperm competition risk

Oppliger

Hosken

Ribi

1998

Proc. R. Soc. Lond. B

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Sperm competition is widespread and in£uences both male investment in spermatogenic tissue and ejaculate characteristics. Sperm competition models assume trade-o¡s between sperm size and number, although such trade-o¡s may be di¤cult to detect. This study examines the e¡ects of sperm competition risk on the sperm production characteristics of the freshwater snail Viviparus ater. In this prosobranch, females mate frequently and store sperm, generating sperm competition. Males produce two sperm morphs, fertile eupyrene sperm and non-fertilizing oligopyrene sperm. Non-fertilizing sperm may play a role in sperm competition and therefore, like fertilizing sperm, the number produced could vary relative to sperm competition risk. In addition, trade-o¡s between sperm number and sperm size may be expected.We manipulated the sex ratio of sexually mature snails and found the presence of rivals a¡ected the ratio of oligopyrene^eupyrene sperm males produced. In experimental and natural populations, the number of oligopyrene sperm produced, but not the number of eupyrene sperm, was signi¢cantly higher when the sex ratio was male biased. Testis mass did not vary between experimental treatments. We also found a negative relationship between the number and size of oligopyrene sperm produced, which is consistent with evolutionary models of sperm competition, and is, to our knowledge, the ¢rst intraspeci¢c demonstration of a trade-o¡ between these traits.

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Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Snail sperm production characteristics vary with sperm competition risk

Oppliger

Hosken

Ribi

1998

Proc. R. Soc. Lond. B

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“…The eupyrene sperm are responsible for egg fertilization, while the apyrene ones, which are devoid of a nucleus, are involved in sperm competition (Drummond, 1984, Silberglied et al, 1984, Gage, 1994, Cook and Wedell, 1996, Cook and Wedell, 1999, Snook, 1997and Snook, 1998. Their ultrastructure is complicated by the presence of exclusive eupyrene appendages, for which the chemical composition and functions are still not elucidated.…”

Section: Discussionmentioning

confidence: 99%

Immunocytochemical localization of tubulins in spermatids and spermatozoa of Euptoieta hegesia (Lepidoptera: Nymphalidae)

et al. 2005

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A comparative analysis of the distribution of tubulin types in apyrene and eupyrene sperm of Euptoieta hegesia butterflies was carried out, also verifying the presence of tubulin in lacinate appendages of the eupyrene sperm. Ultrathin sections of LR White embedded spermatids and spermatozoa were labeled for alpha, beta, gamma, alpha-acetylated and alpha-tyrosinated tubulins. Apyrene and eupyrene spermatids show the same antibody recognition pattern for tubulins. All tubulin types were detected in axonemal microtubules. Alpha and gamma tubulins were also detected on the cytoplasmic microtubules. However, for beta and tyrosinated tubulins only scattered labeling was detected on cytoplasmic microtubules and acetylated tubulin was not detected. In apyrene and eupyrene spermatozoa only the axoneme labeling was analyzed since cytoplasmic microtubules no longer exist in these cells. Alpha, beta and tyrosinated tubulins were easily detected on the apyrene and eupyrene axoneme; gamma tubulin was strongly marked on eupyrene axonemes but was scattered on the apyrene ones. Acetylated tubulin appeared with scattered labeling on the axoneme of both sperm types. Our results demonstrate significant differences in tubulin distribution in apyrene and eupyrene axonemal and cytoplasmic microtubules. Extracellular structures, especially the lacinate appendages, were not labeled by antibodies for any tubulin.

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“…Nevertheless, many invertebrates produce special nonnucleate or partly nonnucleate apyrene "sperm," which are often so distinctive that there seems little question but that they could have functions in addition to fertilization (Baccetti and Afzelius, 1976;Silberglied et al, 1984;Sivinski, 1984). They thus differ from the abnormal sperm of mammals, which seem merely to be variations of the normal sperm.…”

mentioning

confidence: 99%

Sperm Competition and the Evolution of Nonfertilizing Sperm in Mammals

Harcourt

1991

Evolution

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Abstract.-Nonfertilizing sperm with special morphologies have long been known to exist in invertebrates. Until recently, abnormal sperm in mammals were considered errors in production. Now, however, Baker andBellis (1988, 1989) have proposed that mammalian sperm, like some invertebrate sperm, are polymorphic and adapted to a variety of nonfertilizing roles in sperm competition, including prevention of passage of sperm inseminated by another male. More specifically, their "kamikaze" sperm hypothesis proposes that deformed mammalian sperm are adapted to facilitate the formation and functioning of copulatory plugs (Baker and Bellis, 1988). Here I argue that most, maybe all, mammals are unlikely to produce nonfertilizing sperm. First, mammals might not be able to afford to evolve nonfertilizing sperm, given that a) fertilization is often unlikely despite the huge numbers of sperm produced; b) production of larger numbers of sperm is constrained, presumably because ofmetabolic costs, evidence for which includes the fact that in species in which sperm morphology and anatomy ofthe female reproductive tract increase the probability of fertilization, the numbers of sperm produced is lower than in others; and c) selection appears to act against the production of deformed sperm. Second, some of the evidence advanced for the existence ofnon fertilizing sperm does not in fact support the idea. Third, accessory gland secretions are sufficient on their own to coagulate semen and produce fully functioning plugs; thus the male that used accessory gland secretions would be at a clear advantage over the male that diluted his fertilizing sperm with "kamikaze" sperm; and indeed, current evidence indicates selection on accessory glands, not sperm morphology, to enhance coagulation of semen. Fourth, predictions made on the basis of the "kamikaze" sperm hypothesis are not supported by quantitative comparisons of data from polyandrous and monandrous primates (i.e., those in which several males mate with a fertile female, and therefore in which sperm competition should be operating, and those in which only one male mates). Although sperm competition is almost certainly more intense in polyandrous genera than in monandrous genera (as indicated by, e.g., more frequent copulations and the production of more sperm per ejaculate from larger spermatogenic organs), polyandrous genera do not produce a greater proportion of deformed (i.e., nonfertilizing) sperm than do monandrous genera, or even necessarily a greater number of deformed sperm; nor a greater variety of sperm sizes-indeed they might produce fewer; nor fewer motile sperm (as might be expected if sperm are selected to stay behind and compete with sperm from subsequent males); and nor larger sperm (as might be expected if sperm are produced for functions other than to reach the egg). In sum, currently available evidence suggests that the function of all mammalian sperm is to fertilize, and that sperm competition in mammals occurs through scramble competition, not contest competition.

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Eunuchs: The Role of Apyrene Sperm in Lepidoptera?

Cited by 205 publications

References 44 publications

Snail sperm production characteristics vary with sperm competition risk

Snail sperm production characteristics vary with sperm competition risk

Immunocytochemical localization of tubulins in spermatids and spermatozoa of Euptoieta hegesia (Lepidoptera: Nymphalidae)

Sperm Competition and the Evolution of Nonfertilizing Sperm in Mammals

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