ABSTRACT
Sexually selected weapons used to monopolize mating opportunities are predicted to trade-off with traits used in competition for fertilization. Yet, the limited size range typically found among adults of a species often precludes clear comparisons between population-level and individual-level relative trait investment. The jousting weevil, Brentus anchorago (Coleoptera: Brentidae), varies more than 26-fold in body mass, which is among the most extreme adult body size ranges of any solitary terrestrial species. We reveal a trade-off at a population level: hypermetric scaling in male weapons (slopeâ =â 1.59) and a closely mirrored reversal in allocation to postcopulatory traits (slopeâ =â 0.54). Yet, at the individual level, we find the opposite pattern; males that invest relatively more in weapons for their size class also invest more in postcopulatory traits. Across 36 dung beetle and 41 brentine weevil species, we find the allometric slope explains more trait variation at larger body size ranges; in brentines, population-level scaling patterns become more detectable in species with a larger range in adult body size. Our findings reveal that population-level allometries and individual-level trade-offs can both be important in shaping relative trait allocation; we highlight that the adult body size range is rarely examined but may be integral to gaining a deeper understanding of trade-offs in reproductive allocation.
Subject(s)
Body Size , Weevils , Animals , Male , Weevils/physiology , Weevils/anatomy & histology , Female , Mating Preference, Animal , Coleoptera/physiology , Coleoptera/anatomy & histology , Sexual SelectionABSTRACT
The Social Intelligence Hypothesis (SIH) is one of the leading explanations for the evolution of cognition. Since its inception a vast body of literature investigating the predictions of the SIH has accumulated, using a variety of methodologies and species. However, the generalisability of the hypothesis remains unclear. To gain an understanding of the robustness of the SIH as an explanation for the evolution of cognition, we systematically searched the literature for studies investigating the predictions of the SIH. Accordingly, we compiled 103 studies with 584 effect sizes from 17 taxonomic orders. We present the results of four meta-analyses which reveal support for the SIH across interspecific, intraspecific and developmental studies. However, effect sizes did not differ significantly between the cognitive or sociality metrics used, taxonomy or testing conditions. Thus, support for the SIH is similar across studies using neuroanatomy and cognitive performance, those using broad categories of sociality, group size and social interactions, across taxonomic groups, and for tests conducted in captivity or the wild. Overall, our meta-analyses support the SIH as an evolutionary and developmental explanation for cognitive variation.
ABSTRACT
Extensive research has investigated the relationship between the social environment and cognition, suggesting that social complexity may drive cognitive evolution and development. However, evidence for this relationship remains equivocal. Group size is often used as a measure of social complexity, but this may not capture intraspecific variation in social interactions. Social network analysis can provide insight into the cognitively demanding challenges associated with group living at the individual level. Here, we use social networks to investigate whether the cognitive performance of wild Western Australian magpies (Gymnorhina tibicen dorsalis) is related to group size and individual social connectedness. We quantified social connectedness using four interaction types: proximity, affiliative, agonistic and vocal. Consistent with previous research on this species, individuals in larger groups performed better on an associative learning task. However, social network position was also related to cognitive performance. Individuals receiving aggressive interactions performed better, while those involved in aggressive interactions with more group members performed worse. Overall, this suggests that cognitive performance is related to specific types of social interaction. The findings from this study highlight the value of considering fine-grained metrics of sociality that capture the challenges associated with social life when testing the relationship between the social environment and cognition.
Subject(s)
Aggression , Cognition , Social Behavior , Animals , Western Australia , Male , Passeriformes/physiology , FemaleABSTRACT
In species where females compete for mates, the male often provides the female with resources in addition to gametes. A recently suggested definition of sexual selection proposed that if females only benefit from additional resources that come with each mating and not additional gametes, female intrasexual competition for mating opportunities would result in natural selection rather than sexual selection. The nuptial gift-giving bushcricket Kawanaphila nartee has dynamic sex roles and has been a textbook example of sexual selection acting on females via mating competition. We investigated whether females of this species gain fitness benefits from nuptial gifts, additional ejaculates or both by controlling the number of matings and whether the female was allowed to consume the nutritious gift (spermatophylax) at mating. We found that egg production per day of life increased with the number of additional matings, both with and without spermatophylax consumption, but consuming the spermatophylax had an additional positive effect on the number of eggs. These effects were particularly strong in females with shorter lifespans. We discuss how the recently suggested definition of sexual selection applies to nuptial-feeding insects and conclude that both natural and sexual selections influence mating competition in K. nartee females.
ABSTRACT
The ecosystem services provided by dung beetles are well known and valued. Dung beetles bury dung for feeding and breeding, and it is generally thought that the process of burying dung increases nutrient uptake by plant roots, which promotes plant growth. Many studies have tested the effects of dung beetles on plant growth, but there has been no quantitative synthesis of these studies. Here we use a multi-level meta-analysis to estimate the average effect of dung beetles on plant growth and investigate factors that moderate this effect. We identified 28 publications that investigated dung beetle effects on plant growth. Of these, 24 contained the minimum quantitative data necessary to include in a meta-analysis. Overall, we found that dung beetles increased plant growth by 17%; the 95% CI for possible values for the true increase in plant growth that were most compatible with our data, given our statistical model, ranged from 1% to 35%. We found evidence that the dung beetle-plant growth relationship is influenced by the plant measurement type and the number of beetles accessing the dung. However, beetles did not increase plant growth in all quantitative trials, as individual effect sizes ranged from -72% to 806%, suggesting important context-dependence in the provision of ecosystem services.
Subject(s)
Coleoptera , Ecosystem , Animals , Plant Breeding , Plants , FecesABSTRACT
Individual differences in cognitive performance can have genetic, social and environmental components. Most research on the heritability of cognitive traits comes from humans or captive non-human animals, while less attention has been given to wild populations. Western Australian magpies (Gymnorhina tibicen dorsalis, hereafter magpies) show phenotypic variation in cognitive performance, which affects reproductive success. Despite high levels of individual repeatability, we do not know whether cognitive performance is heritable in this species. Here, we quantify the broad-sense heritability of associative learning ability in a wild population of Western Australian magpies. Specifically, we explore whether offspring associative learning performance is predicted by maternal associative learning performance or by the social environment (group size) when tested at three time points during the first year of life. We found little evidence that offspring associative learning performance is heritable, with an estimated broad-sense heritability of just -0.046 ± 0.084 (confidence interval: -0.234/0.140). However, complementing previous findings, we find that at 300 days post-fledging, individuals raised in larger groups passed the test in fewer trials compared with individuals from small groups. Our results highlight the pivotal influence of the social environment on cognitive development.
ABSTRACT
Animal genitalia are thought to evolve rapidly and divergently in response to sexual selection. Studies of genital evolution have focused largely on male genitalia. The paucity of work on female genital morphology is probably due to problems faced in quantifying shape variation, due to their composition and accessibility. Here we use a combination of micro-computed tomography, landmark free shape quantification and phylogenetic analysis to quantify the rate of female genital shape evolution among 29 species of Antichiropus millipedes, and their coevolution with male genitalia. We found significant variation in female and male genital shape among species. Male genital shape showed a stronger phylogenetic signal than female genital shape, although the phylogenetic signal effect sizes did not differ significantly. Male genital shape was found to be evolving 1.2 times faster than female genital shape. Female and male genital shape exhibited strong correlated evolution, indicating that genital shape changes in one sex are associated with corresponding changes in the genital shape of the other sex. This study adds novel insight into our growing understanding of how female genitalia can evolve rapidly and divergently, and highlights the advantages of three-dimensional techniques and multivariate analyses in studies of female genital evolution.
Subject(s)
Arthropods , Biological Evolution , Animals , Male , Female , Phylogeny , X-Ray Microtomography , Genitalia, Male/anatomy & histology , Genitalia, Female/anatomy & histology , Arthropods/anatomy & histologyABSTRACT
Increased expenditure on the ejaculate is a taxonomically widespread male response to sperm competition. Increased ejaculate expenditure is assumed to come at a cost to future reproduction, otherwise males should always invest maximally. However, the life-history costs of strategic ejaculation are not well documented. Macronutrient intake is known to affect the trade-off between reproduction and lifespan. Intakes of protein and carbohydrate that maximize reproduction often differ from those that maximize lifespan. Here, we asked whether strategic expenditure on the ejaculate by male crickets, Teleogryllus oceanicus, is mediated by macronutrient intake, and whether it comes at a cost of reduced lifespan. Males were exposed to rival song throughout their lifespan or were held in a silent non-competitive environment. Males exposed to song had a higher intake of both protein and carbohydrate, they reached adulthood sooner, produced ejaculates of higher quality, and died sooner than males living in a silent environment. Our findings provide a rare example of both the mechanisms and life-history costs associated with strategic ejaculation.
Subject(s)
Semen , Spermatozoa , Animals , Male , Spermatozoa/physiology , Semen/physiology , Longevity , Sexual Behavior, Animal/physiology , Ejaculation/physiology , Eating , CarbohydratesABSTRACT
When females mate with more than one male, competition between rival ejaculates is expected to favor adaptations that promote fertilization success. There is now compelling evidence that sperm competition selects for increased production and allocation of sperm. However, sperm comes packaged in ejaculates that also contain protein-rich seminal fluids. Predicting how males should allocate individual seminal fluid proteins in response to sperm competition is hampered by our limited knowledge of their precise function. We use gene expression studies and interference RNA to ask how seminal fluid proteins in the ejaculate of a cricket, Teleogryllus oceanicus, affect a male's paternity share when in competition for fertilizations. We find that the relative expression of one seminal fluid gene, gagein, positively affects the paternity share of competing males and that knockdown of this and two other seminal fluid protein genes renders males mating in the offensive role of sperm competition incapable of fathering living offspring. Despite having a negative effect on offspring viability these seminal fluid genes have been found to be up regulated in response to rival males, consistent with a role in promoting competitive fertilization success. Our data contribute to a growing body of evidence that, like sperm, seminal fluid gene expression is subject to post-mating sexual selection via sperm competition.
ABSTRACT
Our understanding of genital evolution comes largely from studies of male genitalia. Females have received far less attention because of the difficulties inherent in quantifying the shapes of their internal genital structures. Here we combine advances in micro-computed tomography with a new landmark free method of quantifying three-dimensional trait shape, to document patterns of divergence in female genital shape, and the correlated divergence of male genitalia among populations of the millipede Antichiropus variabilis. We used single-nucleotide polymorphisms to estimate levels of neutral genetic divergence among seven populations of millipede. Genetic divergence was high and correlated with geographic distance. Comparing phenotypic divergence in genital shape to neutral genetic divergence, we found that genital shape for both females and males has diverged more than would be expected from random drift, consistent with a pattern of directional selection. While there was significant covariation between female and male genital shape across populations, the magnitude of divergence in genital shape between the sexes was not correlated. Our results demonstrate the utility of using three-dimensional scanning technologies to examine female genital traits and add to a small but growing number of studies showing that like male genitalia, female genitalia can be under strong directional selection.
Subject(s)
Genitalia, Male , Genitalia , Male , Female , Humans , X-Ray Microtomography , Genitalia/anatomy & histology , Genitalia, Male/anatomy & histology , Genitalia, Female/anatomy & histology , Evolution, Molecular , Biological EvolutionABSTRACT
Global declines in insect abundance are of significant concern. While there is evidence that climate change is contributing to insect declines, we know little of the direct mechanisms responsible for these declines. Male fertility is compromised by increasing temperatures, and the thermal limit to fertility has been implicated as an important factor in the response of insects to climate change. However, climate change is affecting both temperature and hydric conditions, and the effects of water availability on male fertility have rarely been considered. Here we exposed male crickets Teleogryllus oceanicus to either low or high-humidity environments while holding temperature constant. We measured water loss and the expression of both pre- and postmating reproductive traits. Males exposed to a low-humidity environment lost more water than males exposed to a high-humidity environment. A male's cuticular hydrocarbon profile (CHC) did not affect the amount of water lost, and males did not adjust the composition of their CHC profiles in response to hydric conditions. Males exposed to a low-humidity environment were less likely to produce courtship song or produced songs of low quality. Their spermatophores failed to evacuate and their ejaculates contained sperm of reduced viability. The detrimental effects of low-humidity on male reproductive traits will compromise male fertility and population persistence. We argue that limits to insect fertility based on temperature alone are likely to underestimate the true effects of climate change on insect persistence and that the explicit incorporation of water regulation into our modeling will yield more accurate predictions of the effects of climate change on insect declines.
ABSTRACT
Studies of socially mediated phenotypic plasticity have demonstrated adaptive male responses to the 'competitive' environment. Despite this, whether variation in the paternal social environment also influences offspring reproductive potential in an intergenerational context has not yet been examined. Here, we studied the descendants of wild-caught house mice, a destructive pest species worldwide, to address this knowledge gap. We analysed traits that define a 'competitive' phenotype in the sons of males (sires) that had been exposed to either a high-male density (competitive) or high-female density (non-competitive) environment. We report disparate reproductive strategies among the sires: high-male density led to a phenotype geared for competition, while high-female density led to a phenotype that would facilitate elevated mating frequency. Moreover, we found that the competitive responses of sires persisted in the subsequent generation, with the sons of males reared under competition having elevated sperm quality. As all sons were reared under common-garden conditions, variation in their reproductive phenotypes could only have arisen via nongenetic inheritance. We discuss our results in relation to the adaptive advantage of preparing sons for sperm competition and suggest that intergenerational plasticity is a previously unconsidered aspect in invasive mammal fertility control.
Subject(s)
Semen , Spermatozoa , Animals , Mice , Male , Female , Spermatozoa/physiology , Reproduction , Adaptation, Physiological , Mammals , Sexual Behavior, AnimalABSTRACT
Bateman gradients, the slope of the regression of reproductive success on mating success, are among the most commonly reported measures of sexual selection. They are particularly insightful in species with reversed sex roles, where females are expected to be under sexual selection. We measured Bateman gradients in replicate experimental populations of the spermatophore gift-giving bushcricket Kawanaphila nartee (Orthoptera: Tettigoniidae). In this species, the operational sex ratio (OSR) and thus the sex competing for mates varies depending on the availability of pollen food resources: under pollen-limited regimens females are more competitive, whereas under pollen-rich regimens males are more competitive. We maintained populations in enclosures with either limited or supplemented pollen and calculated Bateman gradients for males and females under both conditions. Bateman gradients were significantly positive in males, and the slope was steeper in pollen-supplemented populations where the OSR was more male-biased. Bateman gradients for females were shallow and nonsignificant regardless of pollen availability. Our results show that the strength of sexual selection on males can depend on environmental context. The lack of significant gradients among females may reflect experimental limitations on our ability to estimate Bateman gradients in female K nartee.
Subject(s)
Mating Preference, Animal , Sexual Selection , Animals , Female , Gender Role , Male , Reproduction , Sex Ratio , Sexual Behavior, AnimalABSTRACT
The often complex cocktails of hydrocarbon compounds found on the cuticles of insects can serve both naturally and sexually selected functions, contributing to an individual's ability to withstand water loss and attract mating partners. However, whether natural and sexual selection act synergistically or antagonistically on a species' cuticular hydrocarbon (CHC) profile remains unclear. Here, we examined the ontogeny of the CHC profile in a species of cricket, Teleogryllus oceanicus, while manipulating humidity during development. We predicted that juvenile crickets should produce only those compounds that contribute to desiccation resistance, while those compounds contributing specifically to male attractiveness should be produced only at sexual maturity. Further, if attractive CHCs come at a cost to desiccation resistance as predicted by some models of sexual selection, then males reared under low humidity should be constrained to invest less in attractive CHCs. Crickets reared under low humidity produced more long-chain methyl-branched alkanes, alkenes and alkadienes than did crickets reared under high humidity. The abundance of n-alkanes was unaffected by humidity treatment. Sexual dimorphism in the CHC profile was not apparent until adult emergence and became exaggerated 10â days after emergence, when crickets were sexually mature. Males produced more of the same compounds that were increased in both sexes under low humidity, but the humidity treatment did not interact with sex in determining CHC abundance. The data suggest that CHC profiles which protect crickets from desiccation might have synergistic effects on male attractiveness, as there was no evidence to suggest males trade-off a CHC profile produced in response to low humidity for one associated with sexual signalling.
Subject(s)
Mating Preference, Animal , Alkanes , Animals , Female , Hydrocarbons , Male , Sex Characteristics , Sexual SelectionABSTRACT
In many animal species, males may exhibit one of several discrete, alternative ways of obtaining fertilisations, known as alternative reproductive tactics (ARTs). Males exhibiting ARTs typically differ in the extent to which they invest in traits that improve their mating success, or the extent to which they face sperm competition. This has led to the widespread prediction that males exhibiting ARTs associated with a high sperm competition risk, or lower investment into traits that improve their competitiveness before mating, should invest more heavily into traits that improve their competitiveness after mating, such as large ejaculates and high-quality sperm. However, despite many studies investigating this question since the 1990s, evidence for differences in sperm and ejaculate investment between male ARTs is mixed, and there has been no quantitative summary of this field. Following a systematic review of the literature, we performed a meta-analysis examining how testes size, sperm number and sperm traits differ between males exhibiting ARTs that face either a high or low sperm competition risk, or high or low investment in traits that increase mating success. We obtained data from 92 studies and 67 species from across the animal kingdom. Our analyses showed that male fish exhibiting ARTs facing a high sperm competition risk had significantly larger testes (after controlling for body size) than those exhibiting tactics facing a low sperm competition risk. However, this effect appears to be due to the inappropriate use of the gonadosomatic index as a body-size corrected measure of testes investment, which overestimates the difference in testes investment between male tactics in most cases. We found no significant difference in sperm number between males exhibiting different ARTs, regardless of whether sperm were measured from the male sperm stores or following ejaculation. We also found no significant difference in sperm traits between males exhibiting different ARTs, with the exception of sperm adenosine triphosphate (ATP) content in fish. Finally, the difference in post-mating investment between male ARTs was not influenced by the extent to which tactics were flexible, or by the frequency of sneakers in the population. Overall, our results suggest that, despite clear theoretical predictions, there is little evidence that male ARTs differ substantially in investment into sperm and ejaculates across species. The incongruence between theoretical and empirical results could be explained if (i) theoretical models fail to account for differences in overall resource levels between males exhibiting different ARTs or fundamental trade-offs between investment into different ejaculate and sperm traits, and (ii) studies often use sperm or ejaculate traits that do not reflect overall post-mating investment accurately or affect fertilisation success.
Subject(s)
Reproduction , Semen , Animals , Body Size , Ejaculation , Fishes , Male , Sexual Behavior, Animal , SpermatozoaABSTRACT
Sexually antagonistic coevolution can drive the evolution of male traits that harm females, and female resistance to those traits. While males have been found to vary their harmfulness to females in response to social cues, plasticity in female resistance traits remains to be examined. Here, we ask whether female seed beetles Callosobruchus maculatus are capable of adjusting their resistance to male harm in response to the social environment. Among seed beetles, male genital spines harm females during copulation and females might resist male harm via thickening of the reproductive tract walls. We develop a novel micro computed tomography imaging technique to quantify female reproductive tract thickness in three-dimensional space, and compared the reproductive tracts of females from populations that had evolved under high and low levels of sexual conflict, and for females reared under a social environment that predicted either high or low levels of sexual conflict. We find little evidence to suggest that females can adjust the thickness of their reproductive tracts in response to the social environment. Neither did evolutionary history affect reproductive tract thickness. Nevertheless, our novel methodology was capable of quantifying fine-scale differences in the internal reproductive tracts of individual females, and will allow future investigations into the internal organs of insects and other animals.
Subject(s)
Coleoptera , Animals , Biological Evolution , Female , Genitalia, Female , Genitalia, Male , Male , Sexual Behavior, Animal , X-Ray MicrotomographyABSTRACT
Sperm cells have undergone an extraordinarily divergent evolution among metazoan animals. Parker recognized that because female animals frequently mate with more than one male, sexual selection would continue after mating and impose strong selection on sperm cells to maximize fertilization success. Comparative analyses among species have revealed a general relationship between the strength of selection from sperm competition and the length of sperm cells and their constituent parts. However, comparative analyses cannot address causation. Here, we use experimental evolution to ask whether sexual selection can drive the divergence of sperm cell phenotype, using the dung beetle Onthophagus taurus as a model. We either relaxed sexual selection by enforcing monogamy or allowed sexual selection to continue for 20 generations before sampling males and measuring the total length of sperm cells and their constituent parts, the acrosome, nucleus, and flagella. We found differences in the length of the sperm cell nucleus but no differences in the length of the acrosome, flagella, or total sperm length. Our data suggest that different sperm cell components may respond independently to sexual selection and contribute to the divergent evolution of these extraordinary cells.
Subject(s)
Biological Evolution , Cell Shape , Coleoptera/physiology , Sexual Selection , Spermatozoa/physiology , Animals , Female , Male , Phenotype , Reproduction , Sex CharacteristicsABSTRACT
Studies of fertilization biology often focus on sperm and egg interactions. However, before gametes interact, mammalian sperm must pass through the cumulus layer; in mice, this consists of several thousand cells tightly glued together with hyaluronic acid and other proteins. To better understand the role of cumulus cells and their extracellular matrix, we perform proteomic experiments on cumulus oophorus complexes (COCs) in house mice (Mus musculus), producing over 24,000 mass spectra to identify 711 proteins. Seven proteins known to stabilize hyaluronic acid and the extracellular matrix were especially abundant (using spectral counts as an indirect proxy for abundance). Through comparative evolutionary analyses, we show that three of these evolve rapidly, a classic signature of genes that influence fertilization rate. Some of the selected sites overlap regions of the protein known to impact function. In a follow-up experiment, we compared COCs from females raised in two different social environments. Female mice raised in the presence of multiple males produced COCs that were smaller and more resistant to dissociation by hyaluronidase compared to females raised in the presence of a single male, consistent with a previous study that demonstrated such females produced COCs that were more resistant to fertilization. Although cumulus cells are often thought of as enhancers of fertilization, our evolutionary, proteomic, and experimental investigations implicate their extracellular matrix as a potential mediator of fertilization outcomes.
Subject(s)
Cumulus Cells/physiology , Extracellular Matrix/physiology , Fertilization/physiology , Mice/physiology , Proteome , Animals , Biological Evolution , Female , Fertilization/geneticsABSTRACT
In polyandrous species, males face reproductive competition both before and after mating. Sexual selection thus shapes the evolution of both pre- and postcopulatory traits, creating competing demands on resource allocation to different reproductive episodes. Traits subject to strong selection exhibit accelerated rates of phenotypic divergence, and examining evolutionary rates may inform us about the relative importance and potential fitness consequences of investing in traits under either pre- or postcopulatory sexual selection. Here, we used a comparative approach to assess evolutionary rates of key competitive traits in two artiodactyl families, bovids (family Bovidae) and cervids (family Cervidae), where male-male competition can occur before and after mating. We quantified and compared evolutionary rates of male weaponry (horns and antlers), body size/mass, testes mass, and sperm morphometrics. We found that weapons evolve faster than sperm dimensions. In contrast, testes and body mass evolve at similar rates. These results suggest strong, but differential, selection on both pre- and postcopulatory traits in bovids and cervids. Furthermore, we documented distinct evolutionary rates among different sperm components, with sperm head and midpiece evolving faster than the flagellum. Finally, we demonstrate that, despite considerable differences in weapon development between bovids and cervids, the overall evolutionary patterns between these families were broadly consistent.