Mechanisms of sperm competition in birds: mathematical models

Summary We built models of sperm competition and compared their predictions with observations from domestic chickens in an attempt to elucidate the mechanism of sperm competition. The models suggest that (1) observed levels of precedence of sperm are not merely a passive consequence of the greater mortality of sperm from earlier inseminations; (2) displacement of existing sperm from sperm storage tubules by incoming sperm explains observed levels of sperm precedence and disappearance from the reproductive tract, even in the absence of recognition of sperm from different inseminations; (3) stratification of sperm within the sperm storage tubules fails as an explanation of observed patterns of sperm precedence and disappearance because long-term levels of sperm precedence as high as those observed can only be predicted in combination with rates of disappearance of sperm much lower than those observed in chickens. The predictions of sperm precedence levels following multiple inseminations also suggest that displacement rather than stratification is the most likely mechanism of sperm competition in chickens. We discuss the consequences of male or female control of sperm competition, non-uniform distribution of sperm between sperm storage tubules, and variation in sperm precedence with time after the last insemination, and suggest ways in which the models may be used in future to aid in the elucidation of mechanisms of sperm competition. Offprint requests to: C.M. Lessells     

Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations

Spermatozoa vary greatly in size and shape among species across the animal kingdom. Postcopulatory sexual selection is thought to be the major evolutionary force driving this diversity. In contrast, less is known about how sperm size varies among populations of the same species. Here, we investigate geographic variation in sperm size in barn swallows Hirundo rustica, a socially monogamous passerine with a wide Holarctic breeding distribution. We included samples from seven populations and three subspecies: five populations of ssp. rustica in Europe (Czech, Italy, Norway, Spain, and Ukraine), one population of ssp. transitiva in Israel, and one population of ssp. erythrogaster in Canada. All sperm traits (head length, midpiece length, tail length, and total length) varied significantly among populations. The variation among the European rustica populations was much lower than the differences among subspecies, indicating that sperm traits reflect phylogenetic distance. We also performed a test of the relationship between the coefficient of between-male variation in total sperm length and extrapair paternity levels across different populations within a species. Recent studies have found a strong negative relationship between sperm size variation and extrapair paternity among species. Here, we show a similar negative relationship among six barn swallow populations, which suggests that the variance in male sperm length in a population is shaped by the strength of stabilizing postcopulatory sexual selection.     

Studies on the fusion reaction in two species of Perophora (Ascidiacea)

Histological and electron microscopical studies were made on the fusion reaction between homogeneic stolons of the colonial ascidians Perophora japonica Oka and P. sagamiensis Tokioka. When two stolons make a tip-to-side contact, the epidermal cells of the lateral portion of one stolon become thick and form a protrusion. In the fusion reaction of P. japonica, epidermal cells of each stolon at the contact area extend cell processes immediately after contact. After an occurrence of degenerated epidermal cells, blood interchange between the two stolons is initiated by a partial elimination of the epidermal cells. Even after the establishment of blood interchange, the cuticlelike structure is often observed to remain at the contact area. In the fusion reaction of P. japonica, many amoebocytes are attached to the epidermal cells until the complete elimination of epidermal cells. In the fusion reaction of P. sagamiensis, many lymphocytes as well as amoebocytes are attached to the epidermal cells at the contact area.Contribution No. 461 of the Shimoda Marine Research Center     

Mating behavior and sperm competition in the fly,Dryomyza anilis

Summary Mating behavior in D. andis was studied both in nature and in the laboratory. Each mating in nature consisted of several repeated copulation and oviposition bouts during which the male stayed mounted. One copulation bout included an intromission in the beginning followed by several tapping sequences. During one tapping sequence the male touched the external genitalia of the female with his claspers several times. The experimental matings with irradiated sterile males contained one copulation bout after which the female laid her eggs. In these matings the percentage fertilization for the last male to mate with the female increased with increasing number of tapping sequences. The percentage fertilization was affected positively also by the time between the end of the copulation bout and the start of oviposition, but the time spent in the copulation bout was not important. Furthermore, there was a negative correlation between the length of intromission and the percentage fertilization. After the copulation bout, the percentage fertilization was higher among the first eggs laid. This difference between the first and later eggs laid increased with the increasing number of tapping sequences, suggesting that copulating and ovipositing in several bouts further increase the male percentage fertilization. In matings recorded in nature, both the number of tapping sequences and the number of copulation and oviposition bouts varied greatly. Of the variables recorded during these matings, individual size and the number of eggs the female contained in the beginning of a mating affected the number of copulation bouts and the number of tapping sequences. Males also mated differently with females containing immature or mature eggs. The male behavior resulting in sperm precedence and the variability of matings in nature in relation to male sperm competition is discussed.     

Testes mass in megachiropteran bats varies in accordance with sperm competition theory

Sperm competition is a widespread phenomenon influencing a range of characters, including investment in gonadal tissue. Conspecific proximity is one factor which can influence the risk of sperm competition and hence testicular investment, and decreased confidence of paternity may be one cost of group living. Aspects of female biology may also influence spermatogenic investment and sperm morphology. This study examines the associations between relative testes mass and roost-group size across 17 species of Megachiroptera. Associations between breeding season duration and investment in spermatogenesis are also examined, as are associations between female reproductive tract dimensions and testes mass and dimensions of spermatozoa across all bats. Relative testes mass was significantly positively associated with roost-group size at a species level and after appropriate phylogenetic control (pairwise comparisons and comparison of independent contrasts). There were no significant relationships between breeding season duration and relative testes mass. Across all bats, neither testes mass nor sperm length were significantly related to dimensions of the female tract. The results are discussed in the context of sperm competition. Received: 7 January 1998 / Accepted after revision: 8 August 1998     

Sperm transfer and storage in relation to sperm competition in Callosobruchus maculatus

This paper examines the underlying mechanisms of sperm competition in the beetle Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). Recently developed mathematical models of sperm competition are combined with an empirical investigation of the processes of sperm transfer and storage. During a single insemination virgin males transfer approximately 46000 sperm, 85% more sperm than females can effectively store in their spermathecae. Many of these sperm remain in the bursa copulatrix where they are apparently rapidly degraded and can therefore play no role in fertilization. The spermatheca (primary site of sperm storage) is filled by a single insemination and sperm are lost from this organ at a constant rate. This rate of sperm loss from the spermatheca is insufficient for sperm mixing (without displacement) or sperm stratification to account for the degree of last male sperm precedence measured as P ₂; the proportion of offspring fathered by the second male to mate reported for this species (P ₂ = 0.83, when two inseminations are separated by 24 h). Models of sperm displacement correctly predict high levels of sperm precedence although the precision of these predictions is limited because the proportion of sperm entering the spermatheca cannot be accurately determined. The results suggested that last male sperm precedence in C. maculatus the result of sperm displacement, although the exact mechanism of displacement (sperm-for-sperm or fluid displacement) remains unknown. Possible constraints imposed by female genital anatomy on sperm displacement are discussed.     

Copulatory tactics in relation to sperm competition in Rocky Mountain bighorn sheep

Summary Sperm competition arises in the bighorn mating system because receptive ewes are some-times defended and mated in sequence by a series of increasingly dominant rams and because subordinate (coursing) rams commonly succeed in forcing matings with defended ewes. To identify potential components in a male strategy of sperm competition, the social circumstances and schedule of copulation among free-ranging bighorns were investigated. Three such components emerged: (i) Defending and coursing rams copulated with estrous ewes at extraordinarily high rates, presumably to increase the proportion of their own versus rivals' sperm present at fertilization by simple numerical preponderance at insemination. (ii) Coursing but not defending rams concentrated copulations later in the period of estrus (sensu this study). Evidence from domestic sheep suggests that this may correspond to the period of maximum female fertility. A greater risk and/or reduced benefit associated with forced versus cooperative copulation may force coursing rams to restrict copulation to periods of highest fertility, whereas defending rams may gain even from copulations outside this period. (iii) Defending rams copulated at unusually high rates immediately after bouts of successful coursing. Such retaliatory copulations were associated with reduced amounts of courtship and were more likely to occur if the defending ram had copulated infrequently recently. The number of retaliatory copulations was independent of the number of preceding forced copulations, probably because defending rams rationed ejaculates in anticipation of future coursing. The function of retaliation is not clear, although the literature on domestic sheep suggests the possibility of some form of mechanical displacement of rival sperm. Unlike females of many ungulate species, bighorn ewes were typically receptive to cooperative copulation over a period of days. Although persistent courtship by defending rams may coerce such extended receptivity, it is also possible that ewes, facing unavoidable forced matings by coursing rams, gain genotypic benefits for offspring by providing prolonged copulatory access to relatively dominant defending rams.     

Analysing sperm competition data: simple models for predicting mechanisms

Summary Prospective models are developed for analysing sperm competition data so as to predict the underlying mechanisms determining paternity in multiply mated females. The models require: 1) estimations of proportion of offspring sired by the last male to mate (P ₂), 2) knowledge of the number of sperm transferred by each male, and 3) knowledge of the sperm storage capacity of the female, should this be limited. They will distinguish between raffles (sperm mixing without displacement) and sperm displacement mechanisms. The sensitivity of the techniques can be increased by manipulating the number of sperm transferred by each male. Typically, this can be done by manipulating copula duration or number of ejaculations, given a knowledge of the rate of sperm transfer. Data from two contrasting insect species are fitted to the models to demonstrate the techniques. These models are prospective only, and their limitations are discussed. The principal limitation is that we assume that sperm used for fertilization mix randomly in a fertilization set immediately prior to fertilization; in reality this may be difficult to identify. When sperm mixing is very rapid, the fertilization set will often be equivalent to the sperm stores, but with slow mixing, the fertilization set may be equivalent to a much more restricted zone and may change with time. Offprint requests to: G.A. Parker     

Sperm competition affects sex allocation but not sperm morphology in a flatworm

Sperm competition has been shown to be an important evolutionary agent affecting the behaviour, physiology, and morphology of both males and females. One morphological trait that is particularly likely to be affected by sperm competition is sperm size because it is thought to influence the competitiveness of sperm by determining sperm longevity, motility, and/or their ability to displace competing sperm. Most comparative studies across taxa have found a positive relationship between the level of sperm competition and sperm length, but very few studies have tested for a phenotypically plastic adjustment of sperm morphology in response to sperm competition. In this study, we experimentally tested for an effect of sperm competition on phenotypic plasticity in sperm morphology in an obligately outcrossing simultaneous hermaphrodite, the free-living flatworm Macrostomum lignano, by either raising worms in monogamous pairs (no sperm competition) or in promiscuous groups (intense sperm competition). Worms in groups produced larger testes and smaller ovaries as predicted by sex allocation theory and as previously documented in this species. However, we found no evidence for an effect of group size on sperm morphology, measured as total sperm length, sperm body length, and the length of two different sperm appendages. We conclude that M. lignano may either be incapable of adjusting the sperm morphology in a phenotypically plastic way and/or that there might be no benefit of phenotypic plasticity in sperm traits in this species.     

Male crickets increase sperm number in relation to competition and female size

There is evidence to suggest that males of various species can respond to the threat of sperm competition by varying the amount of sperm transferred during copulation. We tested this in two species of cricket, Acheta domesticus and Gryllodes supplicans (Orthoptera: Gryllidae) by varying the apparent threat of intermale competition experimentally. The results showed that males of both species increased the amount of sperm transferred as apparent competition increased and that male A. domesticus transferred more sperm when encountering larger females. The results also showed that male G. supplicans produced a larger spermatophylax when a larger ampulla was transferred, a relationship consistent with a sperm protection function. Received: 5 May 1995/Accepted after revision: 27 January 1996     

Sperm traits of the quacking frog, Crinia georgiana: intra- and interpopulation variation in a species with a high risk of sperm competition

Sperm traits often show extreme variation both between and within species. Between-species variation may often be interpreted in the context of a sperm competition theory, but within-species variation has remained unexplained. Previous studies on intraspecific variation in sperm traits have focused on a limited set of variables and may have failed to explain observed variation because of potential trade-offs between different sperm traits. We report on variation in number, size, motility and longevity of sperm in the frog Crinia georgiana, a species where sperm competition is common. We found intrapopulation variation in sperm size and motility and interpopulation variation in relative sperm number and size. When we combined relative sperm number and size into one variable, and motility and longevity into another, we found significant interpopulation variation in these variables as well. We also detected considerable intra- and significant interpopulation variation in cumulative sperm quality, a combination of all four sperm traits. Furthermore, a significant effect of the interaction between population origin and male size on sperm characteristics indicated interpopulation variation in the strength of selection acting on sperm traits of males adopting different mating strategies. We discuss heterogeneity in the reproductive environment, a complex genetic background in the determination of sperm characteristics and varying levels of developmental noise as potential contributors to the observed variation in sperm traits.     

Extra-pair paternity,sperm competition and the evolution of testis size in birds

Sperm competition should select for increased sperm production if the probability of fertilization by a specific male is proportional to the relative number of sperm inseminated. A review of the literature generally supports the predicted positive association between sperm production or allocation and various measures of the presumed intensity of sperm competition. However, it is not clear how increased sperm competition is related to extra-pair paternity, and it remains unknown whether certainty of paternity should be associated with relative testis size. Based on a large sample of bird species with information on extra-pair paternity gathered from the literature, we demonstrate that testis mass is related positively to the level of extra-pair paternity, after controlling for body size and phylogeny. Although large testes may be necessary to avoid sperm depletion in species in which males frequently engage in multi-pair copulations, we argue that selection has favoured increased testis mass in situations of more intense sperm competition in order to retaliate against copulations by rival males. The fact the males are not always successful in retaliating against rival ejaculates further suggests that females may largely control the allocation of paternity in birds and that increased sperm production by males may simply be a male strategy to make the best of a bad situation.     

Effects of maternal nutrition on post-weaning growth in two North American rodents

The Trivers-Willard hypothesis of sex-biased maternal investment in response to fluctuations in resource availability has provided a theoretical foundation for research on maternal investment for more than two decades. Their hypothesis holds that mothers in poor condition as a result of poor resource availability should bias parental investment towards offspring with the highest probability of reproducing. In the polygynous mating system of mammals where males compete for breeding access to females, the hypothesis predicts investment favoring females. Although data from many systems have supported this hypothesis, other systems do not follow the predicted patterns and have resulted in various alternative hypotheses. The present research was designed to test whether differences in body condition of young reared by nutritionally stressed dams relative to young reared by unstressed dams were maintained into adulthood, one of the fundamental assumptions underlying the Trivers-Willard hypothesis. Post-weaning growth in eastern woodrats (Neotoma floridana) and northern grasshopper mice (Onychomys leucogaster) was examined relative to maternal nutritional plane. Individuals from undernourished dams were lighter than their unrestricted counterparts at weaning but no difference was evident by the time they had reached adult size. Failure to maintain body condition differences into adulthood violates one of the assumptions essential for application of the Trivers-Willard hypothesis of maternal investment patterns. Although the Trivers-Willard model proposed that natural selection favors differential investment in the sexes over the entire course of parental investment, evidence from this and other studies suggests that the Trivers-Willard hypothesis might not be appropriate to address maternal investment questions in postnatally malnourished dams, but instead should be restricted to systems concerned with prenatal maternal condition or resource availability. Received: 22 February 1995/Accepted after revision: 30 December 1995     

Male capacity as related to sperm production,pregnancy initiation,and sperm competition in deer mice (Peromyscus maniculatus)

Summary Limitations on male capacity may be important to the evolution of mating strategies and behavior. Sperm counts in successive ejaculates of deer mice (Peromyscus maniculatus) decreased progressively through six ejaculations and remained depressed the following day. Males were as effective in inseminating females in cycling estrus with their second two ejaculates as with their first two and as effective in inseminating postpartum females with their fifth as with their first. In sperm competition situations males competed with rested males as effectively with their fourth, fifth, and sixth ejaculates as with their first. Thus, although sperm counts decrease in successive ejaculates, males suffer no apparent functional deficiency as long as they continue ejaculating. It is not clear whether or not deer mice are honest salesmen but they appear to be honest ejaculators and usually are honest intromitters.     

Behavioral aspects of sperm competition in cuttlefish, Sepia officinalis (Sepioidea: Cephalopoda)

Sexual selection studies in cephalopods indicate that sperm competition is a central feature of their mating systems, yet this has not been studied experimentally in any detail. In 1998 we staged 20 matings of the cuttlefish, Sepia officinalis L., in the laboratory. Males rapidly initiated mating in the “head-to-head” position, with no apparent courtship. Mating lasted an average of 10 min (range 7 to 14 min). For the first 6 min (on average 63% of the mating duration), the male flushed strong jets of water directly at the female's buccal membrane, which sometimes resulted in the expulsion of parts of spermatangia placed there in recent matings. Then, in a single discrete movement that lasted an average of only 14 s, the male's modified fourth left arm – the hectocotylus – wrapped around a single large bundle of spermatophores (ca. 150 to 300) and transferred them to the female's buccal membrane. For the remainder of the mating (average 3 min, range 1.5 to 5.0 min), the hectocotylus repeatedly broke the spermatophores open, and manipulated them, so that sperm were released and many spermatangia were attached along the ventral buccal membrane, near the paired seminal receptacles. Approximately 140 spermatangia were attached in rows 3 to 5 deep around the ventral buccal membrane in a single mating; the rest were usually discarded during mating. Histology revealed that each of the seminal receptacles consists of a series of sperm storage bulbs connected by a central duct, which leads to a single pore at the surface of the buccal membrane. Baseline data on sperm motility were obtained, but the mechanism by which sperm enter the seminal receptacle remains unknown. Females seemed to initiate termination of mating, then males guarded their mates temporarily. These results, combined with other recent laboratory experiments, provide evidence that sperm competition may be a major feature of the mating system of S. officinalis. Received: 4 January 1999 / Accepted: 18 May 1999     

Female mediation of sperm competition in the millipede Alloporus uncinatus (Diplopoda: Spirostreptidae)

The tropical spirostreptid millipede Alloporus uncinatus has a polygynandrous mating pattern that is apparently shaped by sperm competition (Telford and Dangerfield 1990, 1993a). In the present study radioisotopic labelling of ejaculates was used to quantify the temporal effects of double mating sequences on sperm precedence patterns. Ejaculates of successive males mix completely within the sperm storage organs and are concentrated close to the site of fertilisation, the spermathecal-oviduct junction. When matings follow each other immediately (experiment 1), equal volumes of the ejaculates of each male are stored within the spermathecae, and both males have equal probability of paternity. Where matings are separated by a 24-h delay (experiment 2), the volumetric contribution of the first male is reduced by 54.8 % and last male precedence operates. Although the distal ends of the gonopods play a primary role in the redistribution of ejaculates (Barnett and Telford 1994), by using a single mating sequence we show that they are not responsible for the reduction in ejaculate volume. The most likely explanation is absorption and/or ejection of the first male's ejaculate by the female. Genital functional morphology is used to reconstruct the mechanism of ejaculate distribution.