THE EVOLUTION OF SPERM SIZE IN BIRDS

Sperm size varies enormously among species, but the reasons for this variation remain obscure. Since it has been suggested that swimming velocity increases with sperm length, earlier studies proposed longer (and therefore faster) sperm are advantageous under conditions of intense sperm competition. Nonetheless, previous work has been equivocal, perhaps because the intensity of sperm competition was measured indirectly. DNA profiling now provides a more direct measure of the number of offspring sired by extrapair males, and thus a more direct method of assessing the potential for sperm competition. Using a sample of 21 species of passerine birds for which DNA profiling data were available, we found a positive relation between sperm length and the degree of extrapair paternity. A path analysis, however, revealed that this relationship arises only indirectly through the positive relationship between the rate of extrapair paternity and length of sperm storage tubules (SSTs) in the female. As sperm length is correlated positively with SST length, an increase in the intensity of sperm competition leads to an increase in sperm length only through its effect on SST length. Why females vary SST length with the intensity of sperm competition is not clear, but one possibility is that it increases female control over how sperm are used in fertilization. Males, in turn, may respond on an evolutionary time scale to changes in SST size by increasing sperm length to prevent displacement from rival sperm. Previous theoretical analyses predicting that sperm size should decrease as sperm competition becomes more intense were not supported by our findings. We suggest that future models of sperm-size evolution consider not only the role of sperm competition, but also how female control and manipulation of ejaculates after insemination selects for different sperm morphologies.     

COMPARATIVE EVIDENCE FOR THE EVOLUTION OF SPERM SWIMMING SPEED BY SPERM COMPETITION AND FEMALE SPERM STORAGE DURATION IN PASSERINE BIRDS

Sperm swimming speed is an important determinant of male fertility and sperm competitiveness. Despite its fundamental biological importance, the underlying evolutionary processes affecting this male reproductive trait are poorly understood. Using a comparative approach in a phylogenetic framework, we tested the predictions that sperm swim faster with (1) increased risk of sperm competition, (2) shorter duration of female sperm storage, and (3) increased sperm length. We recorded sperm swimming speed in 42 North American and European free-living passerine bird species, representing 35 genera and 16 families. We found that sperm swimming speed was positively related to the frequency of extrapair paternity (a proxy for the risk of sperm competition) and negatively associated with clutch size (a proxy for the duration of female sperm storage). Sperm swimming speed was unrelated to sperm length, although sperm length also increased with the frequency of extrapair paternity. These results suggest that sperm swimming speed and sperm length are not closely associated traits and evolve independently in response to sperm competition in passerine birds. Our findings emphasize the significance of both sperm competition and female sperm storage duration as evolutionary forces driving sperm swimming speed.     

Sperm morphology and sperm velocity in passerine birds

Sperm velocity is one of the main determinants of the outcome of sperm competition. Since sperm vary considerably in their morphology between and within species, it seems likely that sperm morphology is associated with sperm velocity. Theory predicts that sperm velocity may be increased by enlarged midpiece (energetic component) or flagellum length (kinetic component), or by particular ratios between sperm components, such as between flagellum length and head size. However, such associations have rarely been found in empirical studies. In a comparative framework in passerine birds, we tested these theoretical predictions both across a wide range of species and within a single family, the New World blackbirds (Icteridae). In both study groups, sperm velocity was influenced by sperm morphology in the predicted direction. Consistent with theoretical models, these results show that selection on sperm morphology and velocity are likely to be concomitant evolutionary forces.     

THE LIKELIHOOD OF SPERM COMPETITION IN MANATEES-EXPLAINING AN APPARENT PARADOX

Florida manatees ( Trichechus manatus latirostris ) are promiscuous, with multiple males mating with individual females. This suggests manatees are sperm competitors. Surprisingly, manatee testes are not relatively large. For adult males in non-winter, testicular size is approximately twice what is expected, based on allometry, for "typical" ( i. e. , non-sperm competitor) male mammals of similar size; for these manatees, combined testicular weight represents 0.19% of the body weight ( n = 27 manatees). Testicular weight was generally largest in manatees older than 7 yr in non-winter. Testicular size of some sperm competitors is as much as an order of magnitude (or more) larger than expected in a "typical" species. Perhaps in compensation for the testes not being remarkably large, the seminal vesicles of mature manatees may be larger than the testes. Production of notably large volumes of seminal fluid characterizes sperm competitor primate species and may have positive energy consequences for species such as the manatee that have extremely low metabolic rates. Another possible explanation for the observed relationship between testicular mass and body mass in manatees is that selection for a greatly expanded hindgut and extremely dense, heavy integument could make the body mass of manatees "artificially" high, and the relative testicular mass "artificially" low.     

SPERM COMPETITION PROMOTES ASYMMETRIES IN REPRODUCTIVE BARRIERS BETWEEN CLOSELY RELATED SPECIES

Reproductive barriers between closely related species are often incomplete and asymmetric, but the evolutionary significance of these well-known phenomena remains unsolved. We test the hypothesis that the degree of gametic incompatibility in reciprocal crosses is associated to levels of sperm competition because this selective force favors both increased sperm competitiveness and ovum defensiveness. Using three species of Mus with high, intermediate, and low levels of sperm competition, we examined fertilization rates in competitive and noncompetitive contexts. We found that the influence of sperm competition upon sperm competitiveness is as strong as it is upon ovum defensiveness, revealing an effect upon female gametes so far overlooked. As a result, fertilization success was strongly related to differences in sperm competition levels between species providing sperm and ova, thus generating major asymmetries in reciprocal crosses. When placed in competition, conspecific sperm maintained levels of fertilization success similar to those found in noncompetitive contexts, at the expense of the success of heterospecific sperm. When only heterospecific sperm competed, species with highest levels of sperm competition outcompeted others and asymmetries were exacerbated. We conclude that sperm competition explains both the degree of gametic isolation and the degree of asymmetries between closely related species.     

INDIVIDUAL VARIATION IN SPERM COMPETITION SUCCESS OF YELLOW DUNG FLIES,SCATOPHAGA STERCORARIA

Intraspecific variation in the proportion of offspring sired by the second male to mate with a female (P₂) is an aspect of sperm competition that has received little attention. We examined variation in the sperm competition success of individual male dung flies, Scatophaga stercoraria. In unmanipulated matings, copula duration was dependent on male size with smaller males copulating for longer. A principal component analysis was used to generate uncorrelated scores based on a male's size and copula duration. Using these scores demonstrated that P₂ values were dependent both on the relative size and copula durations of competing males. When copula duration was held constant, the success of an individual male increased as his body size, relative to the first male, increased. We interrupted copulations of “large” and “small” second males and fitted the resultant P₂ values to a linear model of sperm competition with unequal ejaculates. The data fit well to a model of sperm displacement in which sperm mix quickly on introduction to the sperm stores. Furthermore, they show that “large” males have a greater rate of sperm displacement than “small” males. The levels of prey availability during testis maturation may influence a male's success in sperm competition although his immediate mating history does not. We show why an understanding of variation in sperm competition success is important for understanding the mechanisms and evolutionary significance of sperm competition.     

SPERM MORPHOLOGY AND VELOCITY ARE GENETICALLY CODETERMINED IN THE ZEBRA FINCH

Sperm morphology (size and shape) and sperm velocity are both positively associated with fertilization success, and are expected to be under strong selection. Until recently, evidence for a link between sperm morphology and velocity was lacking, but recent comparative studies have shown that species with high levels of sperm competition have evolved long and fast sperm. It is therefore surprising that evidence for a phenotypic or genetic relationship between length and velocity within species is equivocal, even though sperm competition is played out in the intraspecific arena. Here, we first show that sperm velocity is positively phenotypically correlated with measures of sperm length in the zebra finch Taeniopygia guttata . Second, by using the quantitative genetic "animal model" on a dataset from a multigenerational-pedigreed population, we show that sperm velocity is heritable, and positively genetically correlated to a number of heritable components of sperm length. Therefore, selection for faster sperm will simultaneously lead to the evolution of longer sperm (and vice versa). Our results provide, for the first time, a clear phenotypic and genetic link between sperm length and velocity, which has broad implications for understanding how recently described macroevolutionary patterns in sperm traits have evolved.     

EJACULATE QUALITY AND CONSTRAINTS IN RELATION TO SPERM COMPETITION LEVELS AMONG EUTHERIAN MAMMALS

The outcome of sperm competition is influenced by the relative quantity and quality of sperm among competing ejaculates. Whereas it is well established that individual ejaculate traits evolve rapidly under postcopulatory sexual selection, little is known about other factors that might influence the evolution of ejaculates. For example, the metabolic rate is likely to affect the sperm production rate and the cellular activity or metabolism of sperm, and it has recently been suggested to constrain the evolution of sperm length in large but not small mammals. I thus examined in eutherian mammals how ejaculate quality traits vary with one another and with testis mass, body size, and metabolism. I found all ejaculate traits to covary positively with one another and to increase with relative testis mass. When controlling for testis mass, small‐bodied species showed superior sperm quality (but not sperm number). Furthermore, sperm motility and viability were positively associated with the mass‐corrected metabolic rate, but the percentage of morphologically normal and acrosome‐intact sperm were not. These results indicate that body size and the energy budget may also influence the evolution of ejaculate quality, although these influences appear to vary among traits.     

SPERMATOPHORE SIZE IN BUSHCRICKETS: COMPARATIVE EVIDENCE FOR NUPTIAL GIFTS AS A SPERM PROTECTION DEVICE

During courtship and copulation, males of many insect species provide the female with a nuptial gift of a prey item or synthesized material. These gifts may be explained as a form of paternal investment by increasing female reproductive output, or in terms of mating effort by increasing male fertilization success. These explanations, while not mutually exclusive, are controversial. While experimental studies examine the maintenance of nuptial gifts in single species, comparative studies are required to indicate more general evolutionary trends. Male bushcrickets provide females with a nuptial gift, a spermatophylax, which is transferred to females at mating along with the sperm-containing ampulla. Analysis of comparative data of 28 species of bushcrickets (Orthoptera: Tettigoniidae), reveals that male spermatophore size (spermatophylax and ampulla weight) is positively correlated with female refractory period, which, in turn, correlates with male fertilization success. Moreover, gift size (the spermatophylax) covaries with ejaculate size (the ampulla), which is consistent with the hypothesis that it serves as a sperm protection device. In contrast, there is no significant correlation between any measure of female fecundity and male spermatophylax size. This indicates that the variation in spermatophore size among bushcrickets is better explained by a mating-effort function than a paternal investment function.     

SEX ALLOCATION ADJUSTMENT TO MATING GROUP SIZE IN A SIMULTANEOUS HERMAPHRODITE

Sex allocation theory is considered as a touchstone of evolutionary biology, providing some of the best supported examples for Darwinian adaptation. In particular, Hamilton's local mate competition theory has been shown to generate precise predictions for extraordinary sex ratios observed in many separate‐sexed organisms. In analogy to local mate competition, Charnov's mating group size model predicts how sex allocation in simultaneous hermaphrodites is affected by the mating group size (i.e., the number of mating partners plus one). Until now, studies have not directly explored the relationship between mating group size and sex allocation, which we here achieve in the simultaneously hermaphroditic flatworm Macrostomum lignano. Using transgenic focal worms with ubiquitous expression of green‐fluorescent protein (GFP), we assessed the number of wild‐type mating partners carrying GFP+ sperm from these focal worms when raised in different social group sizes. This allowed us to test directly how mating group size was related to the sex allocation of focal worms. We find that the proportion of male investment initially increases with increasing mating group size, but then saturates as predicted by theory. To our knowledge, this is the first direct test of the mating group size model in a simultaneously hermaphroditic animal.     

The evolutionary ecology of testicular function: size isn't everything

Larger testes are considered the quintessential adaptation to sperm competition. However, the strong focus on testis size in evolutionary research risks ignoring other potentially adaptive features of testicular function, many of which will also be shaped by post‐mating sexual selection. Here we advocate a more integrated research programme that simultaneously takes into account the developmental machinery of spermatogenesis and the various selection pressures that act on this machinery and its products. The testis is a complex organ, and so we begin by outlining how we can think about the evolution of testicular function both in terms of the composition and spatial organisation of the testis (‘testicular histology’), as well as in terms of the logical organisation of cell division during spermatogenesis (‘testicular architecture’). We then apply these concepts to ask which aspects of testicular function we can expect to be shaped by post‐mating sexual selection. We first assess the impact of selection on those traits most strongly associated with sperm competition, namely the number and kind of sperm produced. A broad range of studies now support our contention that post‐mating sexual selection affects many aspects of testicular function besides gross testis size, for example, to maximise spermatogenic efficiency or to enable the production of particular sperm morphologies. We then broaden our focus to ask how testicular function is affected by fluctuation in sperm demand. Such fluctuation can occur over an individual's lifetime (for example due to seasonality in reproduction) and may select for particular types of testicular histology and architecture depending on the particular reproductive ecology of the species in question. Fluctuation in sperm demand also occurs over evolutionary time, due to shifts in the mating system, and this may have various consequences for testicular function, for example on rates of proliferation‐induced mutation and for dealing with intragenomic conflict. We end by suggesting additional approaches that could be applied to study testicular function, and conclude that simultaneously considering the machinery, products and scheduling of spermatogenesis will be crucial as we seek to understand more fully the evolution of this most fundamental of male reproductive traits.     

EXPERIMENTAL MANIPULATION OF SEXUAL SELECTION PROMOTES GREATER MALE MATING CAPACITY BUT DOES NOT ALTER SPERM INVESTMENT

Sexual selection theory makes clear predictions regarding male spermatogenic investment. To test these predictions we used experimental sexual selection in Drosophila pseudoobscura , a sperm heteromorphic species in which males produce both fertile and sterile sperm, the latter of which may function in postmating competition. Specifically, we determined whether the number and size of both sperm types, as well as relative testis mass and accessory gland size, increased with increased sperm competition risk and whether any fitness benefits could accrue from such changes. We found no effect of sexual selection history on either the number or size of either sperm morph, or on relative testis mass. However, males experiencing a greater opportunity for sexual selection evolved the largest accessory glands, had the greatest mating capacity, and sired the most progeny. These findings suggest that sterile sperm are not direct targets of sexual selection and that accessory gland size, rather than testis mass, appears to be an important determinant of male reproductive success. We briefly review the data from experimental sexual selection studies and find that testis mass may not be a frequent target of postcopulatory sexual selection and, even when it is, the resulting changes do not always improve fitness.     

PRONOUNCED WITHIN‐INDIVIDUAL PLASTICITY IN SPERM MORPHOMETRY ACROSS SOCIAL ENVIRONMENTS

Sperm morphometry (i.e., size and shape) and function are important determinants of male reproductive success and are thought to be under stabilizing selection. However, recent studies suggest that sperm morphometry can be a phenotypically plastic trait, which can be adjusted to varying conditions. We tested whether different behavioral strategies in aggression between aggressive red and nonaggressive black males of the color polymorphic Gouldian finch (Erythrura gouldiae) can influence sperm morphometry. We show pronounced within‐individual phenotypic plasticity in sperm morphometry of male Gouldian finches in three different social environments. Both red and black males placed in intermediate to high competitive environments (high frequency of red males) increased the relative length of their sperm midpiece. By contrast, red males placed in low to intermediate competitive environments (higher frequency of black males) increased the length of the sperm flagellum. Significant changes in stress and sex steroid hormone levels (in response to the competitive environment) appear to influence sperm traits in red but not in black males, suggesting that changes in hormonal levels are not solely responsible for the observed changes in sperm morphometry. These findings imply that males can adjust sperm morphometry across social environments.     

The Azores bullfinch (Pyrrhula murina) has the same unusual and size‐variable sperm morphology as the Eurasian bullfinch (Pyrrhula pyrrhula)

The Azores bullfinch is endemic to the island of São Miguel in the Azores archipelago and the sister species to the Eurasian bullfinch. Here we show that the spermatozoa of the two species have similar ultrastructure and gross morphology. Thus, the unusual and supposedly neotenous sperm morphology previously described for the Eurasian bullfinch appears to be an ancestral trait that evolved before the two taxa diverged. In addition, the coefficients of variation in total sperm length, both within and among males, were high in both species and exceed any previously published values for free‐living passerines. Such high sperm‐size variation is typically found in species with relaxed sperm competition. However, the high variance in mean sperm length among Azores bullfinches is surprising, because the trait has high heritability and this small, insular population shows clear signs of reduced genetic diversity at neutral loci. A possible explanation for this apparent contradiction is that the Azores bullfinch has retained more diversity at functional and fitness‐related loci than at more neutral parts of the genome. Finally, we also present data on relative testis size and sperm swimming speed for the Eurasian bullfinch, and discuss the hypothesis that the small and putatively neotenous sperm in bullfinches has evolved in response to lack of sperm competition. © 2013 The Linnean Society of London     

THE EVOLUTION OF PLUMAGE BRIGHTNESS IN BIRDS IS RELATED TO EXTRAPAIR PATERNITY

A positive association between plumage brightness of male birds and the degree of polygyny may be the result of sexual selection. Although most birds have a socially monogamous mating system, recent paternity analyses show that many offspring are fathered by nonmates. Extrapair paternity arises from extrapair copulations which are frequently initiated by females. Not all females will be able to mate with a male of the preferred phenotype, because of the mating decisions of earlier paired females; extrapair copulations may be a means for females to adjust their precopulation mate choice. We use two comparative analyses (standardized linear contrasts and pairwise comparisons between closely related taxa) to test the idea that male plumage brightness is related to extrapair paternity. Brightness of male plumage and sexual dimorphism in brightness were positively associated with high levels of extrapair paternity, even when potentially confounding variables were controlled statistically. This association between male brightness and extrapair paternity was considerably stronger than the association between male brightness and the degree of polygyny. Cuckoldry thus forms an important component of sexual selection in birds.     

Determinants of mating and sperm‐transfer success in a simultaneous hermaphrodite

The number of mating partners an individual has within a population is a crucial parameter in sex allocation theory for simultaneous hermaphrodites because it is predicted to be one of the main parameters influencing sex allocation. However, little is known about the factors that determine the number of mates in simultaneous hermaphrodites. Furthermore, in order to understand the benefits obtained by resource allocation into the male function it is important to identify the factors that predict sperm‐transfer success, i.e. the number of sperm a donor manages to store in a mate. In this study we experimentally tested how social group size (i.e. the number of all potential mates within a population) and density affect the number of mates and sperm‐transfer success in the outcrossing hermaphroditic flatworm Macrostomum lignano. In addition, we assessed whether these parameters covary with morphological traits, such as body size, testis size and genital morphology. For this we used a method, which allows tracking sperm of a labelled donor in an unlabelled mate. We found considerable variation in the number of mates and sperm‐transfer success between individuals. The number of mates increased with social group size, and was higher in worms with larger testes, but there was no effect of density. Similarly, sperm‐transfer success was affected by social group size and testis size, but in addition this parameter was influenced by genital morphology. Our study demonstrates for the first time that the social context and the morphology of sperm donors are important predictors of the number of mates and sperm‐transfer success in a simultaneous hermaphrodite. Based on these findings, we hypothesize that sex allocation influences the mating behaviour and outcome of sperm competition.     

SIZE STRUCTURE AND DYNAMICS IN A POPULATION OF SARGASSUM MUTICUM (PHAEOPHYCEAE)

Sargassum muticum (Yendo) Fensholt is an introduced brown seaweed with a very distinctive seasonal growth cycle on European shores. The present study links the dynamics of a population of S. muticum with the seasonal growth cycle of the species and the density-dependent processes operating throughout this cycle. Results indicate that both growth cycle and intraspecific competition influenced the structure and population dynamics. Size inequality increased during the slow growth phase (autumn–winter) of the 2-year study. Mechanisms generating inequality of size could be the existence of asymmetric competition and the inherent differences in growth rates between old (regenerated) and new thalli (recruits). Inequality of size distributions decreased progressively during the last months of the growth phase (spring–summer) and could be related to a process of self-thinning. There was a negative biomass–density relationship (as a measure of biomass accumulation-driven mortality) that confirms the importance of self-thinning as a major demographic factor in the S. muticum population.     

家白蚁群体数增长的生殖生理特点

家白蚁Coptotermes formosanus Shiraki营大巢生活,由于雌虫生殖潜能很大,群体蚁数极多.群体蚁数的逐年增长和雌蚁卵巢内卵巢管的数目增长有密切关系.实验表明,分飞时的雌虫卵巢有8条卵巢管,初建群体,半年内一群体的蚁数仅为57个.经过四年后发育的群体,蚁数是1,767个,这时的蚁后卵巢管数是75条.二年群体的年幼蚁后腹部稍膨大,三年以上的群体,蚁后的1腹部膨大较显著.一年的群体,雌虫体长是0.78厘米,雄虫体长0.71厘米.九年后的群体,蚁后体长是2.1厘米,蚁王体长为1.2厘米.和卵巢相似,雄虫精巢叶的数目也随时间而增加.