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1.
Convergent evolution of sperm gigantism and the developmental origins of sperm size variability in Caenorhabditis nematodes
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Anne Vielle Nicolas Callemeyn‐Torre Clotilde Gimond Nausicaa Poullet Jeremy C. Gray Asher D. Cutter Christian Braendle 《Evolution; international journal of organic evolution》2016,70(11):2485-2503
Sperm cells provide essential, if usually diminutive, ingredients to successful sexual reproduction. Despite this conserved function, sperm competition and coevolution with female traits can drive spectacular morphological change in these cells. Here, we characterize four repeated instances of convergent evolution of sperm gigantism in Caenorhabditis nematodes using phylogenetic comparative methods on 26 species. Species at the extreme end of the 50‐fold range of sperm‐cell volumes across the genus have sperm capable of comprising up to 5% of egg‐cell volume, representing severe attenuation of the magnitude of anisogamy. Furthermore, we uncover significant differences in mean and variance of sperm size among genotypes, between sexes, and within and between individuals of identical genotypes. We demonstrate that the developmental basis of sperm size variation, both within and between species, becomes established during an early stage of sperm development at the formation of primary spermatocytes, while subsequent meiotic divisions contribute little further sperm size variability. These findings provide first insights into the developmental determinants of inter‐ and intraspecific sperm size differences in Caenorhabditis. We hypothesize that life history and ecological differences among species favored the evolution of alternative sperm competition strategies toward either many smaller sperm or fewer larger sperm. 相似文献
2.
S. Lüpold L. W. Simmons J. L. Tomkins J. L. Fitzpatrick 《Journal of evolutionary biology》2015,28(12):2187-2195
Male ornaments and armaments that mediate success in mate acquisition and ejaculate traits influencing competitive fertilization success are under intense sexual selection. However, relative investment in these pre‐ and post‐copulatory traits depends on the relative importance of either selection episode and on the energetic costs and fitness gains of investing in these traits. Theoretical and empirical work has improved our understanding of how precopulatory sexual traits and investments in sperm production covary in this context. It has recently also been suggested that male weapon size may trade off with sperm length as another post‐copulatory sexual trait, but the theoretical framework for this suggestion remains unclear. We evaluated the relationship between precopulatory armaments and sperm length, previously reported in ungulates, in five taxa as well as meta‐analytically. Within and between taxa, we found no evidence for a negative or positive relationship between sperm length and male traits that are important in male–male contest competition. It is important to consider pre‐ and post‐copulatory sexual selection together to understand fitness, and to study investments in different reproductive traits jointly rather than separately. A trade‐off between pre‐ and post‐copulatory sexual traits may not manifest itself in sperm length but rather in sperm number or function. Particularly in large‐bodied taxa such as ungulates, sperm number is more variable interspecifically and likely to be under more intense selection than sperm length. We discuss our and the previous results in this context. 相似文献
3.
Post‐copulatory sexual selection is thought to be responsible for much of the extraordinary diversity in sperm morphology across metazoans. However, the extent to which post‐copulatory selection targets sperm morphology versus sperm production is generally unknown. To address this issue, we simultaneously characterized the evolution of sperm morphology (length of the sperm head, midpiece and flagellum) and testis size (a proxy for sperm production) across 26 species of Anolis lizards, a group in which sperm competition is likely. We found that the length of the sperm midpiece has evolved 2–3 times faster than that of the sperm head or flagellum, suggesting that midpiece size may be the most important aspect of sperm morphology with respect to post‐copulatory sexual selection. However, testis size has evolved faster than any aspect of sperm morphology or body size, supporting the hypothesis that post‐copulatory sexual selection acts more strongly upon sperm production than upon sperm morphology. Likewise, evolutionary increases in testis size, which typically indicate increased sperm competition, are not associated with predictable changes in sperm morphology, suggesting that any effects of post‐copulatory selection on sperm morphology are either weak or variable in direction across anoles. Collectively, our results suggest that sperm production is the primary target of post‐copulatory sexual selection in this lineage. 相似文献
4.
Gomendio M Tourmente M Roldan ER 《Proceedings. Biological sciences / The Royal Society》2011,278(1721):3135-3141
The hypothesis that sperm competition should favour increases in sperm size, because it results in faster swimming speeds, has received support from studies on many taxa, but remains contentious for mammals. We suggest that this may be because mammalian lineages respond differently to sexual selection, owing to major differences in body size, which are associated with differences in mass-specific metabolic rate. Recent evidence suggests that cellular metabolic rate also scales with body size, so that small mammals have cells that process energy and resources from the environment at a faster rate. We develop the 'metabolic rate constraint hypothesis' which proposes that low mass-specific metabolic rate among large mammals may limit their ability to respond to sexual selection by increasing sperm size, while this constraint does not exist among small mammals. Here we show that among rodents, which have high mass-specific metabolic rates, sperm size increases under sperm competition, reaching the longest sperm sizes found in eutherian mammals. By contrast, mammalian lineages with large body sizes have small sperm, and while metabolic rate (corrected for body size) influences sperm size, sperm competition levels do not. When all eutherian mammals are analysed jointly, our results suggest that as mass-specific metabolic rate increases, so does maximum sperm size. In addition, species with low mass-specific metabolic rates produce uniformly small sperm, while species with high mass-specific metabolic rates produce a wide range of sperm sizes. These findings support the hypothesis that mass-specific metabolic rates determine the budget available for sperm production: at high levels, sperm size increases in response to sexual selection, while low levels constrain the ability to respond to sexual selection by increasing sperm size. Thus, adaptive and costly traits, such as sperm size, may only evolve under sexual selection when metabolic rate does not constrain cellular budgets. 相似文献
5.
6.
Stefan Lüpold John L. Fitzpatrick 《Proceedings. Biological sciences / The Royal Society》2015,282(1819)
Postcopulatory sexual selection is widely accepted to underlie the extraordinary diversification of sperm morphology. However, why does it favour longer sperm in some taxa but shorter in others? Two recent hypotheses addressing this discrepancy offered contradictory explanations. Under the sperm dilution hypothesis, selection via sperm density in the female reproductive tract favours more but smaller sperm in large, but the reverse in small, species. Conversely, the metabolic constraint hypothesis maintains that ejaculates respond positively to selection in small endothermic animals with high metabolic rates, whereas low metabolic rates constrain their evolution in large species. Here, we resolve this debate by capitalizing on the substantial variation in mammalian body size and reproductive physiology. Evolutionary responses shifted from sperm length to number with increasing mammalian body size, thus supporting the sperm dilution hypothesis. Our findings demonstrate that body-size-mediated trade-offs between sperm size and number can explain the extreme diversification in sperm phenotypes. 相似文献
7.
Clint D. Kelly Michael D. Jennions 《Biological reviews of the Cambridge Philosophical Society》2011,86(4):863-884
Multiple mating or group spawning leads to post‐copulatory sexual selection, which generally favours ejaculates that are more competitive under sperm competition. In four meta‐analyses we quantify the evidence that sperm competition (SC) favours greater sperm number using data from studies of strategic ejaculation. Differential investment into each ejaculate emerges at the individual level if males exhibit phenotypic plasticity in ejaculate properties in response to the likely risk and/or intensity of sperm competition after a given mating. Over the last twenty years, a series of theoretical models have been developed that predict how ejaculate size will be strategically adjusted in relation to: (a) the number of immediate rival males, with a distinction made between 0 versus 1 rival (‘risk’ of SC) and 1 versus several rivals (‘intensity’ of SC); (b) female mating status (virgin or previously mated); and (c) female phenotypic quality (e.g. female size or condition). Some well‐known studies have reported large adjustments in ejaculate size depending on the relevant social context and this has led to widespread acceptance of the claim that strategic sperm allocation occurs in response to each of these factors. It is necessary, however, to test each claim separately because it is easy to overlook studies with weak or negative findings. Compiling information on the variation in outcomes among species is potentially informative about the relevance of these assumptions in different taxa or mating systems. We found strong evidence that, on average, males transfer larger ejaculates to higher quality females. The effect of female mating status was less straightforward and depended on how ejaculate size was measured (i.e. use of proxy or direct measure). There is strong evidence that ejaculate size increased when males were exposed to a single rival, which is often described as a response to the risk of SC. There is, however, no evidence for the general prediction that ejaculate size decreases as the number of rivals increases from one to several males (i.e. in response to a higher intensity of SC which lowers the rate of return per sperm released). Our results highlight how meta‐analysis can reveal unintentional biases in narrative literature reviews. We note that several assumptions of theoretical models can alter an outcome's predicted direction in a given species (e.g. the effect of female mating status depends on whether there is first‐ or last‐male sperm priority). Many studies do not provide this background information and fail to make strong a priori predictions about the expected response of ejaculate size to manipulation of the mating context. Researchers should be explicit about which model they are testing to ensure that future meta‐analyses can better partition studies into different categories, or control for continuous moderator variables. 相似文献
8.
J.‐F. LEMAÎTRE S. A. RAMM R. A. BARTON P. STOCKLEY 《Journal of evolutionary biology》2009,22(11):2215-2221
The ‘expensive tissue hypothesis’ predicts a size trade‐off between the brain and other energetically costly organs. A specific version of this hypothesis, the ‘expensive sexual tissue hypothesis’, argues that selection for larger testes under sperm competition constrains brain size evolution. We show here that there is no general evolutionary trade‐off between brain and testis mass in mammals. The predicted negative relationship between these traits is not found for rodents, ungulates, primates, carnivores, or across combined mammalian orders, and neither does total brain mass vary according to the level of sperm competition as determined by mating system classifications. Although we are able to confirm previous reports of a negative relationship between brain and testis mass in echolocating bats, our results suggest that mating system may be a better predictor of brain size in this group. We conclude that the expensive sexual tissue hypothesis accounts for little or none of the variance in brain size in mammals, and suggest that a broader framework is required to understand the costs of brain size evolution and how these are met. 相似文献
9.
Salom Bourg Laurent Jacob Frdric Menu Etienne Rajon 《Evolution; international journal of organic evolution》2019,73(4):661-674
Recent empirical evidence suggests that trade‐off relationships can evolve, challenging the classical image of their high entrenchment. For energy reliant traits, this relationship should depend on the endocrine system that regulates resource allocation. Here, we model changes in this system by mutating the expression and conformation of its constitutive hormones and receptors. We show that the shape of trade‐offs can indeed evolve in this model through the combined action of genetic drift and selection, such that their evolutionarily expected curvature and length depend on context. In particular, the shape of a trade‐off should depend on the cost associated with resource storage, itself depending on the traded resource and on the ecological context. Despite this convergence at the phenotypic level, we show that a variety of physiological mechanisms may evolve in similar simulations, suggesting redundancy at the genetic level. This model should provide a useful framework to interpret and unify the overly complex observations of evolutionary endocrinology and evolutionary ecology. 相似文献
10.
Luisana Carballo Alessandra Battistotti Kim Teltscher Michael Lierz Andreas Bublat Mihai Valcu Bart Kempenaers 《Journal of evolutionary biology》2019,32(8):856-867
Sperm competition is an important component of post‐copulatory sexual selection that has shaped the evolution of sperm morphology. Previous studies have reported that sperm competition has a concurrently directional and stabilizing effect on sperm size. For example, bird species that show higher levels of extrapair paternity and larger testes (proxies for the intensity of sperm competition) have longer sperm and lower coefficients of variation in sperm length, both within and between males. For this reason, these sperm traits have been proposed as indexes to estimate the level of sperm competition in species for which other measures are not available. The relationship between sperm competition and sperm morphology has been explored mostly for bird species that breed in temperate zones, with the main focus on passerine birds. We measured sperm morphology in 62 parrot species that breed mainly in the tropics and related variation in sperm length to life‐history traits potentially indicative of the level of sperm competition. We showed that sperm length negatively correlated with the within‐male coefficient of variation in sperm length and positively with testes mass. We also showed that sperm is longer in sexually dichromatic and in gregarious species. Our results support the general validity of the hypothesis that sperm competition drives variation in sperm morphology. Our analyses suggest that post‐copulatory sexual selection is also important in tropical species, with more intense sperm competition among sexually dichromatic species and among species that breed at higher densities. 相似文献
11.
Hanna N. Ststad Melissah Rowe Arild Johnsen Jan T. Lifjeld 《Journal of evolutionary biology》2019,32(7):666-674
Sperm morphology varies enormously across the animal kingdom. Whilst knowledge of the factors that drive the evolution of interspecific variation in sperm morphology is accumulating, we currently have little understanding of factors that may constrain evolutionary change in sperm traits. We investigated whether susceptibility to sperm abnormalities could represent such a constraint in songbirds, a group characterized by a distinctive helical sperm head shape. Specifically, using 36 songbird species and data from light and scanning electron microscopy, we examined among‐species correlations between the occurrence of sperm head abnormalities and sperm morphology, as well as the correlation between sperm head abnormalities and two indicators of sperm competition. We found that species with more helically shaped sperm heads (i.e., a wider helical membrane and more pronounced cell waveform) had a higher percentage of abnormal sperm heads than species with less helical sperm (i.e., relatively straight sperm) and that sperm head traits were better predictors of head abnormalities than total sperm length. In contrast, there was no correlation between sperm abnormalities and the level of sperm competition. Given that songbird species with more pronounced helical sperm have higher average sperm swimming speed, our results suggest an evolutionary trade‐off between sperm performance and the structural integrity of the sperm head. As such, susceptibility to morphological abnormalities may constrain the evolution of helical sperm morphology in songbirds. 相似文献
12.
ALEX CÓRDOBA-AGUILAR 《Biological journal of the Linnean Society. Linnean Society of London》2009,96(4):815-829
Sperm competition is a pervasive force. One adaptation is the male ability to displace the rivals' sperm that females have stored from previous copulations. In the damselfly, Calopteryx haemorrhoidalis asturica , males with wider aedeagi displace more spermathecal sperm. The present study documents that the same mechanism operates in another damselfly, Hetaerina americana . However, this genital width in both species decreases along the season, but late-emerging females have more sperm displaced than early-emerging females. Because territorial males mated more and were larger in body and genital size than nonterritorial males, late-season females mated with considerably larger males with respect to female size and this produced higher sperm displacement. Assuming female benefits from storing sperm but that such benefit does not prevail if males displace sperm, it is predicted that, along the season, females will mate less and male harassment (in terms of male mating attempts and oviposition duration) will increase. These predictions were corroborated. In H. americana , it was also tested whether spermathecal sperm became less viable along the season. The results obtained did not corroborate this. This is the first evidence indicating that season affects sperm displacement ability and female mating frequency due to changes in male body and genital size. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 815–829. 相似文献
13.
As females of many species mate with more than one male, ejaculates often face competition from the sperm of other males. In recent years, numerous papers have been published on theoretical predictions of evolutionary, behavioural and physiological responses to variation in the strength of sperm competition (SC). These theoretical predictions have also been extensively tested. However, although predictions from SC theory are relatively straightforward, extra caution has to be paid in the design of experiments testing them. One difficulty is for example to disentangle immediate and mean SC risk and intensity. Without carefully designed experiments, it is also very easy to simultaneously increase SC risk and the probability of intense SC--a situation for which we currently have no clear predictions, as the theoretical models to date only assume variation in either SC risk or intensity. In this paper, we discuss these and some other pitfalls related to manipulations of SC risk and intensity and suggest how to avoid them. 相似文献
14.
Raúl Cueva del Castillo Salomón Sanabria‐Urbán Martín Alejandro Serrano‐Meneses 《Ecology and evolution》2015,5(18):3914-3926
Trade‐offs between life‐history traits – such as fecundity and survival – have been demonstrated in several studies. In eusocial insects, the number of organisms and their body sizes can affect the fitness of the colony. Large‐than‐average body sizes as well as more individuals can improve a colony's thermoregulation, foraging efficiency, and fecundity. However, in bumblebees, large colonies and large body sizes depend largely on high temperatures and a large amount of food resources. Bumblebee taxa can be found in temperate and tropical regions of the world and differ markedly in their colony sizes and body sizes. Variation in colony size and body size may be explained by the costs and benefits associated with the evolutionary history of each species in a particular environment. In this study, we explored the effect of temperature and precipitation (the latter was used as an indirect indicator of food availability) on the colony and body size of twenty‐one bumblebee taxa. A comparative analysis controlling for phylogenetic effects as well as for the body size of queens, workers, and males in bumblebee taxa from temperate and tropical regions indicated that both temperature and precipitation affect colony and body size. We found a negative association between colony size and the rainiest trimester, and a positive association between the colony size and the warmest month of the year. In addition, male bumblebees tend to evolve larger body sizes in places where the rain occurs mostly in the summer and the overall temperature is warmer. Moreover, we found a negative relationship between colony size and body sizes of queens, workers, and males, suggesting potential trade‐offs in the evolution of bumblebee colony and body size. 相似文献
15.
Pattarini JM Starmer WT Bjork A Pitnick S 《Evolution; international journal of organic evolution》2006,60(10):2064-2080
Contrary to early predictions of sperm competition theory, postcopulatory sexual selection favoring increased investment per sperm (e.g., sperm size, sperm quality) has been demonstrated in numerous organisms. We empirically demonstrate for Drosophila melanogaster that both sperm quality and sperm quantity independently contribute to competitive male fertilization success. In addition to these independent effects, there was a significant interaction between sperm quality and quantity that suggests an internal positive reinforcement on selection for sperm quality, with selection predicted to intensify as investment per sperm increases and the number of sperm competing declines. The mechanism underlying the sperm quality advantage is elucidated through examination of the relationship between female sperm-storage organ morphology and the differential organization of different length sperm within the organ. Our results exemplify that primary sex cells can bear secondary sexual straits. 相似文献
16.
Signal diversification in Oecanthus tree crickets is shaped by energetic,morphometric, and acoustic trade‐offs
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L. B. Symes M. P. Ayres C. P. Cowdery R. A. Costello 《Evolution; international journal of organic evolution》2015,69(6):1518-1527
Physiology, physics, and ecological interactions can generate trade‐offs within species, but may also shape divergence among species. We tested whether signal divergence in Oecanthus tree crickets is shaped by acoustic, energetic, and behavioral trade‐offs. We found that species with faster pulse rates, produced by opening and closing wings up to twice as many times per second, did not have higher metabolic costs of calling. The relatively constant energetic cost across species is explained by trade‐offs between the duration and repetition rate of acoustic signals—species with fewer stridulatory teeth closed their wings more frequently such that the number of teeth struck per second of calling and the resulting duty cycle were relatively constant across species. Further trade‐offs were evident in relationships between signals and body size. Calling was relatively inexpensive for small males, permitting them to call for much of the night, but at low amplitude. Large males produced much louder calls, reaching up to four times more area, but the energetic costs increased substantially with increasing size and the time spent calling dropped to only 20% of the night. These trade‐offs indicate that the trait combinations that arise in these species represent a limited subset of conceivable trait combinations. 相似文献
17.
Sperm competition theory predicts increased spermatogenic investment with increased sperm competition risk when competition is numerical. There is ample correlational evidence for this relationship in a wide range of taxa. However, as with all correlations, this does not establish cause and effect. Nevertheless, there are no published experimental studies of the evolutionary influence of sperm competition on testis size. We report here on evolutionary responses of testis size to variation in sperm competition intensity in the yellow dung fly. Experimental flies were divided across two treatments, polyandrous or monogamous, with four replicates of each. There was a rapid evolutionary response in testis size resulting from selection via sperm competition, with larger testes found when sperm competition intensity was greatest. These results provide direct experimental evidence of evolutionary change consistent with macro‐evolutionary patterns found across a wide range of taxa. 相似文献
18.
Selection and constraints on offspring size‐number trade‐offs in sand lizards (Lacerta agilis)
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G. Ljungström M. Stjernstedt E. Wapstra M. Olsson 《Journal of evolutionary biology》2016,29(5):979-990
The trade‐off between offspring size and number is a central component of life‐history theory, postulating that larger investment into offspring size inevitably decreases offspring number. This trade‐off is generally discussed in terms of genetic, physiological or morphological constraints; however, as among‐individual differences can mask individual trade‐offs, the underlying mechanisms may be difficult to reveal. In this study, we use multivariate analyses to investigate whether there is a trade‐off between offspring size and number in a population of sand lizards by separating among‐ and within‐individual patterns using a 15‐year data set collected in the wild. We also explore the ecological and evolutionary causes and consequences of this trade‐off by investigating how a female's resource (condition)‐ vs. age‐related size (snout‐vent length) influences her investment into offspring size vs. number (OSN), whether these traits are heritable and under selection and whether the OSN trade‐off has a genetic component. We found a negative correlation between offspring size and number within individual females and physical constraints (size of body cavity) appear to limit the number of eggs that a female can produce. This suggests that the OSN trade‐off occurs due to resource constraints as a female continues to grow throughout life and, thus, produces larger clutches. In contrast to the assumptions of classic OSN theory, we did not detect selection on offspring size; however, there was directional selection for larger clutch sizes. The repeatabilities of both offspring size and number were low and we did not detect any additive genetic variance in either trait. This could be due to strong selection (past or current) on these life‐history traits, or to insufficient statistical power to detect significant additive genetic effects. Overall, the findings of this study are an important illustration of how analyses of within‐individual patterns can reveal trade‐offs and their underlying causes, with potential evolutionary and ecological consequences that are otherwise hidden by among‐individual variation. 相似文献
19.
Both gamete competition and gamete limitation can generate anisogamy from ancestral isogamy, and both sperm competition (SC) and sperm limitation (SL) can increase sperm numbers. Here, we compare the marginal benefits due to these two components at any given population level of sperm production using the risk and intensity models in sperm economics. We show quite generally for the intensity model (where N males compete for each set of eggs) that however severe the degree of SL, if there is at least one competitor for fertilization (N − 1 ≥ 1), the marginal gains through SC exceed those for SL, provided that the relationship between the probability of fertilization (F) and increasing sperm numbers (x) is a concave function. In the risk model, as fertility F increases from 0 to 1.0, the threshold SC risk (the probability q that two males compete for fertilization) for SC to be the dominant force drops from 1.0 to 0. The gamete competition and gamete limitation theories for the evolution of anisogamy rely on very similar considerations: our results imply that gamete limitation could dominate only if ancestral reproduction took place in highly isolated, small spawning groups. 相似文献
20.
Oviduct length was measured in 48 species representing 33 genera of mammals in order to examine possible relationships between female morphology and the occurrence of sperm competition due to matings with multiple males. Multiple regression analyses revealed that residuals of oviduct length were positively correlated both with residuals of testes weight and with sperm midpiece volume in the genera and species studied. These correlations remained significant after application of comparative analysis of independent contrasts to control for possible phylogenetic biases in the data set. These results indicate that sexual selection (relating to sperm competition and cryptic female choice) has influenced co-evolution of oviduct length, testes size and sperm morphology in mammals. 相似文献