Evolution of mating systems and sexual size dimorphism in North American cyprinids

Mating systems evolve with sexual size dimorphism (SSD) in many animals. Mating systems with males larger than females occur when males compete for female access or guard territories, while mating systems with group mating tend to occur in species where females are the same size or larger than males. In addition to variation in SSD with mating system, sperm competition varies among mating systems in predictable patterns. We examined the evolution of mating systems with SSD and testes mass in 111 North American Cyprinidae fishes using phylogenetic comparative methods. Our results demonstrate that the evolution of mating systems in Cyprinidae fishes is from ancestral taxa that are group spawners with females the same size or larger than males to pair spawning systems where males tend to be larger than females. We used an additive model to predict male and female body size from testes mass and mating system. Only mating system varied predictably with SSD. Our results for analyses of hyperallometry (Rensch’s rule) were that individual species of Cyprinidae can have hyperallometry for SSD, but the pattern is not present across all taxa.     

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     

Mating patterns and a test for female mate choice in Etheostoma spectabile (Pisces,Percidae)

Neither size nor breeding color correlated with spawning success of male orangethroat darters, Etheostoma spectabile (Pisces, Percidae), under natural field conditions. When females were presented experimentally with a simultaneous choice they spent no more time in proximity to large than small males, and were subsequently no more likely to spawn with large than with small males. Females also displayed no preference for bright versus dull males. Males and females did not differ significantly in size. Etheostoma spectabile may lack sexual size dimorphism as a result of the lack of female choice for size and the ineffectiveness of male attempts to monopolize females, or selection may be for increased size of females. Males are not dwarfs because of sperm competition. Contest competition among males appeared to be important in initiating spawnings but many males obtained spawnings by participating in ongoing spawning events. Etheostoma spectabile is an example of a sexually dimorphic species with no evident female preference for male size or color.     

Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus)

The aim of this study was to investigate reproductive strategies and their consequences in gray mouse lemurs (Microcebus murinus), small solitary nocturnal primates endemic to Madagascar. Previous reports of sexual dimorphism in favor of males and females, respectively, a high potential for sperm competition and pheromonal suppression of mating activity among captive males, led us to investigate mechanisms of intrasexual competition in a wild population. Based on 3 years of mark-recapture data, we demonstrate that sexual dimorphism in this species fluctuated annually as a result of independent changes in male and female body mass. Male body mass increased significantly prior to the short annual mating season. Because their testes increased by 100% in the same period and because their canines are not larger than those of females, we suggest that large male size may be advantageous in searching for estrous females and in enabling them to sustain periods of short-term torpor. In contrast to reports from captive colonies, we found no evidence for two morphologically distinct classes of males. Finally, we also show that most adult males are active throughout the cool dry season that precedes the mating season, whereas most adult females hibernate for several months. This is in contrast to other solitary hibernating mammals, where males typically emerge 1–2 weeks before females. Thus, this first extended field study of M.␣murinus clarified previous conflicting reports on sexual dimorphism and male reproductive strategies in this primitive primate by showing that their apparent deviation from predictions of sexual selection theory is brought about by specific environmental conditions which result in sex-specific life history tactics not previously described for mammals. A general conclusion is that sexual selection can operate more strongly on males without resulting in sexual dimorphism because of independent selection on the same traits in females. Received: 6 July 1997 / Accepted after revision: 28 March 1998     

Sex ratios,mating behavior and sexual size dimorphism of the northern water snake,Nerodia sipedon

Competition among males to mate is generally associated with male-biased size dimorphism. In this study we examine mating behavior in the northern water snake (Nerodia sipedon), a species in which males are much smaller than females despite substantial competition among males to mate. Competition among males was a consequence of a male-biased operational sex ratio due to slightly higher female mortality from a birth sex ratio of 1 : 1, and, in 1 year, more synchronous and longer mating activity by males. Approximately one-third of both males and females appeared not to mate in a given year. Larger males were generally more likely to attempt mating, but size did not explain the variance in the number of aggregations in which individual males participated. Within aggregations, males that were successful at achieving intromission were larger than unsuccessful males in 1 of 2 years. Variation in condition (mass relative to length) and relative tail length were not generally useful predictors of either mating effort or success in males. Because large size was often advantageous to males, sexual size dimorphism appeared not to be a consequence of sexual selection favoring smaller males. Because sexual dimorphism was evident at birth, and both males and females matured sexually at about 4 years, sexual dimorphism was not simply a consequence of one sex growing at the maximum rate for longer. Female fecundity increased with size, and sex differences in size-fecundity relations may underly the pattern of sexual size dimorphism. However, because multiple mating by females is common, sperm competition is likely to be important in determining male reproductive success. Therefore, allocation of energy to sperm rather than growth may also prove to be an important influence on male growth rates and sexual size dimorphism.     

Testes size and breeding systems in Japanese annrans with special reference to large testes in the treefrog,Rhacophorus arboreus (Amphibia : Rhacophoridae)

Summary Testes size was compared among 19 species of Japanese anurans in relation to their breeding systems. Although the mean body mass of the species examined varied markedly between 1.8 and 116 g, the mean proportion of testes mass to body mass was fairly constant at 0.2 to 0.4% across all species except the rhacophorid species. Foam-nest building rhacophorids had relatively large testes constituting more than 1% of their body mass. Among them, Rhacophorus arboreus had the largest, exceeding 5% of the body mass. Multi-male breeding, where a female is grasped by two or more males during spawning, occurs frequently in these rhacophorids, especially in R. arboreus. This close association between large testes size and multi-male breeding strongly suggests that sperm competition is an important factor affecting the evolution of relative testes size in Japanese anurans. Offprint requests to: T. Kusano     

Male sperm reserves and copulation frequency in birds

Summary Male passerine birds store sperm in a cloacal protuberance during the breeding season. We consider three hypotheses to explain interspecific variation in relative cloacal protuberance size. The copulation efficiency hypothesis states that a relatively large cloacal protuberance facilitates sperm transfer and predicts more rapid copulation in species with larger protuberances. There is insufficient data to test this idea rigorously, but we found no evidence for such an effect. The spermatozoa size hypothesis is a non-functional hypothesis which states that cloacal protuberance size is merely a consequence of sperm size, and predicts that species with larger spermatozoa have relatively larger cloacal protuberances. Sperm length was positively correlated with protuberance size, providing support for this hypothesis, although it seems unlikely that variation in sperm size alone is sufficient to account for variation in protuberance size because the numbers of sperm stored in the cloacal protuberance were also positively correlated with its size. The sperm competition hypothesis states that the cloacal protuberance is a sperm store and predicts that when sperm competition is intense, as measured by male copulation frequency and or mating system, males will have relatively large protuberances and testes mass. The sperm competition hypothesis was supported: in a comparative study in which we controlled for phylogenetic effects, relative cloacal protuberance size was significantly and positively correlated with copulation frequency. Across all mating systems protuberance size was also positively correlated with the mass of seminal glomera tissue, the number of sperm stored in the seminal glomera, and with relative testes size. These results suggest that where sperm competition is intense, a large cloacal protuberance is required to maintain a large sperm reserve for a high copulation rate.Correspondence to: T.R. Birkhead     

Testis size variation in frogs: testing the alternatives

While sperm competition may be a major factor affecting relative testis size in vertebrates as a whole, additional hypotheses have not been given much attention in frogs. This is important because sperm competition is relatively uncommon in frogs and relative testis size varies in frogs that do not have multiple-male breeding systems. This paper tests two additional hypotheses for differences in relative testis size among frogs: relative clutch size (number of eggs/snout vent length) and androgen level. Testis size was measured in 90 species of frogs belonging to five families. Relative testis size was found to be positively correlated with relative clutch size in species that lack sperm competition. Mean androgen levels of species also positively covaried with relative testis size. However, there was no correlation between relative testis size and level of male agonistic behavior among species, despite other work indicating that testosterone levels are positively correlated with agonistic behavior in at least some species. These findings suggest that a number of factors in addition to sperm competition are important in the evolution of testis size in male frogs. Received: 17 January 1997 / Accepted after revision: 23 June 1997     

Sperm characteristics associated with different male reproductive tactics in bluegills (Lepomis macrochirus)

We examined the availability and motility of sperm from parental and sneaker male bluegills (Lepomis macrochirus), a colonially nesting sunfish (Family Centrarchidae) with male parental care and a high incidence of cuckoldry by both sneaker and satellite males. We found no differences between sneakers and parentals in length and swimming speed of sperm, or percent and duration of sperm activity. In sneaker milt, however, sperm was almost 50% more concentrated than in parental milt (16.5×10⁶ vs 11.5×10⁶ sperm/μl of milt, respectively). Despite this difference in sperm concentration, stripped ejaculates from sneakers contained almost 400 million fewer sperm (only 32% as many sperm) than those from parentals due to their much smaller stripped ejaculate volumes (only about 19% that of parentals). Thus unless sneakers can compensate by releasing more sperm or gaining closer proximity to eggs at the time of spawning, they may be at a disadvantage with respect to sperm competition. We discuss these results in relation to models for the evolution of alternative reproductive behaviours in this species and suggest that the cuckolders may be making the best of a bad situation. Received: 18 February 2000 / Revised: 23 March 2000 / Accepted: 14 September 2000     

Does delayed fertilization facilitate sperm competition in bats?

Reproductive delays between mating and birth may provide a previously unconsidered avenue for post-copulatory sexual selection in mammals. In particular, delayed fertilization could provide an enhanced opportunity for sperm competition by extending the time for ejaculates to interact in the female reproductive tract. We tested the prediction that species with delayed fertilization exhibit greater degrees of sperm competition than those without delays by examining testis volume (a proxy for sperm competition) in 38 species of bats. Examination of fluid-preserved museum specimens of bat species with and without delays revealed that species with delays (in particular those with delayed fertilization) had significantly larger testes than species without them. Although it predicts the presence of delayed fertilization, hibernation did not predict relative testis size. We conclude that, once they evolve, reproductive delays may facilitate sperm competition.     

Intrasexual selection in Mirza coquereli : evidence for scramble competition polygyny in a solitary primate

The primates of Madagascar (Lemuriformes) deviate from fundamental predictions of sexual selection theory in that polygynous species lack sexual dimorphism, have even adult sex ratios and often live in female-dominated societies. It has been hypothesized that intrasexual selection in these species is either reduced or primarily focused on traits related to scramble competition. The goal of this study was to examine these hypotheses by studying the mating system of a solitary nocturnal species, Mirzacoquereli. During a 4-year field study in western Madagascar, I captured and followed 88 individually marked animals. I found that adult males were significantly larger than females, providing the first evidence for sexual size dimorphism in lemurs. In addition, the adult sex ratio was biased in favour of females in 3 out of 4 years. There was no significant sex difference in canine size, however. Males showed pronounced seasonal variation in testis size with a 5-fold increase before and during the short annual mating season. During the mating season, males had more injuries than females and more than quadrupled their home ranges, overlapping with those of more than ten females, but also with about the same number of rivals. Only about one social interaction per 10 h of observation was recorded, but none of them were matings. Together, these results indicate that these solitary lemurs are clearly subject to intrasexual selection and that male-male competition is primarily, but not exclusively, of the scramble type. In addition, they suggest that the above-mentioned idiosyncracies may be limited to group-living lemurs, that social systems of solitary primates are more diverse than previously thought, and that the temporal distribution of receptive females is responsible for this particular male mating strategy. Received: 11 January 1997 / Accepted after revision: 18 April 1997     

Male characteristics, sperm traits, and reproductive success in winter-spawning Celtic Sea Atlantic herring, Clupea harengus

The relationship between sperm characteristics and reproductive success was examined in male herring, Clupea harengus L. Males were categorised as being first-time or repeat spawners on the basis of their age; they were also grouped according to whether their sperm were immediately active and exhibited forward motion on contact with seawater (FM) or had little or only vibratory motion (VM). Unlike the Pacific herring C. pallasii Valencienes, Atlantic herring sperm is usually motile on contact with seawater. The age, weight and gonadosomatic index (testes mass as a percentage of somatic mass = GSI) were measured and used as characteristics for individual fish. Sperm traits measured were (1) adenosine triphosphate (ATP) concentration, (2) sperm count, (3) duration of sperm motility. Reproductive success for each male was estimated from the fertilisation rate and from the length of larvae at hatching. Fertilisation rates for all fish were generally >80%. The ATP concentration of non-activated spermatozoa was negatively correlated with fertilisation rate. Among repeat spawners, fish with higher GSIs produced larvae that were larger at hatching. Although VM sperm fertilised eggs at rates equivalent to fertilisation by FM sperm, the larvae produced by VM sperm were significantly smaller at hatching. Larval length tended to increase in parallel with the duration of sperm motility, but the relationship was not significant in these tests. The results did not indicate any age or size pattern to spawning readiness in male herring. Sperm that are not yet ready to be shed are not fully motile on contact with seawater, but are still capable of fertilising eggs that hatch successfully. There is likely to be a progression of males which come into spawning readiness within a spawning shoal; therefore it is possible that paternal influences would result in a progressive decrease in larval size over the spawning period in winter-spawning Celtic Sea herring. Received: 22 November 1997 / Accepted: 8 June 1998     

Sexual selection on mature male parr of masu salmon (Oncorhynchus masou): does sneaking behavior favor small body size and less-developed sexual characters?

In many salmonid species, males exhibit morphological dimorphism associated with alternative mating behaviors. ”Precocious males” have a small body size with little or no development of sexual characters and adopt sneaking to gain access to females, while ”migratory males” of large body size and well-developed secondary sexual characters fight. We quantified selection on precocious male parr of masu salmon (Oncorhynchus masou) under simulated natural conditions to examine the contribution of morphology to sneaking success. In contrast to the prediction that sneaking behavior favors small body size, we detected selection favoring relatively large body size for sneaking success. This selection pressure was caused by the dominance hierarchy within parr and may have been facilitated by indifference of dominant migratory males to parr. Unlike the secondary sexual characters exhibited by migratory male salmon, such as the hooked snout and humped back, no morphological characters other than body size contributed to the reproductive success of masu salmon parr. This non-contribution may have been responsible for the lack of development of sexual characters in precocious males. Received: 15 November 1999 / Accepted: 20 May 2000     

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.     

Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (<Emphasis Type="Italic">Tamias amoenus</Emphasis>): implications for sperm competition and reproductive success

Comparative analyses have found that relative testis size is a strong predictor of the prevalence of sperm competition for many taxa, including mammals, yet underlying this pattern is the assumption that intraspecific variation in testis size is related to individual fitness. Because intraspecific variation in ejaculate investment underlies interspecific patterns, it is critical to understand the causes and consequences of intraspecific variation in ejaculate investment. We examined relationships between ejaculate investment (testis size and sperm length) and reproductive success, body size and condition in the yellow-pine chipmunk (Tamias amoenus), a small ground squirrel in which sperm competition occurs. We examined genetic estimates of male reproductive success from a wild population of yellow-pine chipmunks and determined that males with large testes had higher annual reproductive success than males with small testes. This result provides empirical support for the numerous comparative studies that indicate testis size is associated with the intensity of sperm competition. In addition, males in good condition had relatively larger testes than males in poor condition, but there was no evidence of sperm length being dependent on condition. Finally, contrary to many predictions, males that invested more in sperm production (relatively heavy testes) produced shorter sperm, not longer sperm, than males that invested less.Communicated by P.M. Kappeler     

Optimal investment in sons and daughters when parents do not know the sex of their offspring

Optimal parental investment usually differs depending on the sex of the offspring. However, parents in most organisms cannot discriminate the sex of their young until those young are energetically independent. In a species with physical male–male competition, males are often larger and usually develop sexual ornaments, so male offspring are often more costly to produce. However, Onthophagus dung beetles (Coleoptera; Scarabaeidae) are highly dimorphic in secondary sexual characters, but sexually monomorphic in body size, despite strong male–male competition for mates. We demonstrate that because parents provide all resources required by their offspring before adulthood, O. atripennis exhibits no sexual size dimorphism irrespective of sexual selection pressure favoring sexual dimorphism. By constructing a graphic model with three fitness curves (for sons, daughters, and expected fitness return for parents), we demonstrate that natural selection favors parents that provide both sons and daughters with the optimal amount of investment for sons, which is far greater than that for daughters. This is because the cost of producing small sons, that are unable to compete for mates, is far greater than the cost of producing daughters that are larger than necessary. This theoretical prediction can explain sexual dimorphism without sexual size dimorphism, widely observed in species with crucial parental care such as dung beetles and leaf-rolling beetles, and may provide an insight into the enigmatic relationship between sexual size dimorphism and sexual dimorphism.     

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.     

Sexual size dimorphism in fallow deer (Dama dama): do larger, heavier males gain greater mating success?

Sexual size dimorphism may evolve as a result of both natural and sexual selection. In polygynous mammals, the main factor resulting in the evolution of large body size in males is the advantage conferred during competition for mates. In this study, we examined whether sexual selection acts on body size in mature fallow bucks (Dama dama) by examining how the following traits are inter-related: age, body (skeletal) size, body mass, prerut dominance rank, rut dominance rank and mating success. This is the first study to examine how all these factors are together related to the mating success of a large sexually dimorphic and polygynous mammal. We found that male mating success was directly related to body size, but not to body mass. However body mass was related to prerut dominance rank which was in turn strongly related to rut dominance rank, and thus there was an indirect relationship between mating success and body mass. Rut dominance rank was the variable most strongly related to mating success. Mating success among mature males was unrelated to age. We conclude that larger mature fallow bucks have advantages over other males when competing for matings, and sexual selection therefore continues to act on sexual size dimorphism in this species. Heavier fallow bucks also have advantages, but these are mediated through the dominance ranks attained by males before the rut.     

Scramble competition selects for greater tailfin size in male red-spotted newts (Amphibia: Salamandridae)

Darwin predicted that scramble competition for access to reproductive females would result in sexual dimorphism of locomotory structures, but direct evidence for this is extremely rare. I examined the relationship between variation in tailfin size and mating success in a field and laboratory study of red-spotted newts, Notophthalmus viridescens. Over three breeding seasons, male tailfin size was positively correlated with variation in male amplexus frequency, and indirectly correlated with male insemination frequency. In a laboratory study, I confirmed that males' ability to capture females is affected by variation in tailfin size. This is the first study to show that naturally occurring variation in male locomotory structures affects male mating success. It corroborates the prediction that scramble competition leads to sexual selection on locomotory structures and, potentially, to dimorphism in these structures. Received: 16 April 1999 / Received in revised form: 16 May 1999 / Accepted: 12 June 1999