Costs of weaponry: Unarmed males sire more offspring than armed males in a male‐dimorphic mite

Morphological structures used as weapons in male–male competition are not only costly to develop but are also probably costly to maintain during adulthood. Therefore, having weapons could reduce the energy available for other fitness‐enhancing actions, such as post‐copulatory investment. We tested the hypothesis that armed males make lower post‐copulatory investments than unarmed males, and that this difference will be most pronounced under food‐limited conditions. We performed two experiments using the male‐dimorphic bulb mite Rhizoglyphus robini, in which males are either armed “fighters” or unarmed “scramblers.” Firstly, we tested whether fighters and scramblers differed in their reproductive output after being starved or fed for 1 or 2 weeks. Secondly, we measured the reproductive output of scramblers and fighters (starved or fed) after one, two or three consecutive matings. Scramblers sired more offspring than fighters after 1 week, but scramblers and fighters only sired a few offspring after 2 weeks. Scramblers also sired more offspring than fighters at the first mating, and males rarely sired offspring after consecutive matings. Contrary to our hypothesis, the fecundity of starved and fed males did not differ. The higher reproductive output of scramblers suggests that, regardless of nutritional state, scramblers make larger post‐copulatory investments than fighters. Alternatively, (cryptic) female choice generally favours scramblers. Why the morphs differed in their reproductive output is unclear. Neither morph performed well relatively late in life or after multiple matings. It remains to be investigated to what extent the apparent scrambler advantage contributes to the maintenance and evolution of male morph expression.     

Life-history consequences of bidirectional selection for male morph in a male-dimorphic bulb mite

Intralocus sexual conflict (IASC) arises when males and females have different trait optima. Some males pursue different alternative reproductive tactics (ARTs) with different trait optima, resulting in different strengths of IASC. Consequently, for instance daughter fitness is differentially affected by her sire’s morph. We tested if—and which—other life-history traits correlatively change in bidirectional, artificial selection experiments for ARTs. We used the male-dimorphic bulb mite Rhizoglyphus robini, the males of which are high-fitness ‘fighters’ or low-fitness ‘scramblers’. Twice in each of the five generations of selection, we assessed clutch composition (number of mites of the various life stages present) and size (total number of offspring). Furthermore, we tracked offspring from egg to adulthood in the first and final generation to detect differences between selection lines in the size and duration of stages, and in maturation time. We found that selection for male morph increased the frequency of that morph. Furthermore, compared to fighter lines, scrambler lines produced more females, which laid larger eggs (in the final generations), and maintained a higher egg-laying rate for longer. Otherwise, our results showed no consistent differences between the selection lines in clutch size and composition, life stage size or duration, or maturation time. Though we found few correlated life-history trait changes in response to selection on male morph, the differences in egg laying rate and egg size suggest that IASC between fighters is costlier to females than IASC with scramblers. We hypothesize that these differences in reproductive traits allow fighter-offspring to perform better in small, declining populations but scrambler-offspring to perform better in large, growing populations.     

Effects of variation in nutrition on male morph development in the bulb mite Rhizoglyphus robini

In male dimorphic species, growth influences morph expression and thereby the reproductive success of males. However, how variation in nutritional conditions affects male morph development and whether males can compensate for lost growth is poorly known. Here, we performed an experiment where males of the bulb mite (Rhizoglyphus robini)—which are fighters, able to kill other mites, or benign scramblers—were offered high quality food during the larval stage, but food of high or low quality during the protonymph and tritonymph (=final) stage. When food quality was low during the latter two stages, males matured smaller, later and were more likely to be a scrambler than when food quality was high. We found no evidence for compensatory growth: when males had low quality food only during the protonymph stage, they matured at the same age, but grew at a slower rate and matured at a smaller size than males that had high quality food throughout ontogeny. Furthermore, males that experienced this transient period of low food quality were less likely to mature as a fighter. Interestingly, scrambler increase in body size during the protonymph and tritonymph stages was always lower than that of fighters. Given the strong link between adult size and fitness, combined with the different development times and life histories of the male morphs, the lack of ability to compensate for a transient period of food deprivation during ontogeny is likely to have consequences for the dynamics of bulb mite populations.     

SELECTION FOR ALTERNATIVE MALE REPRODUCTIVE TACTICS ALTERS INTRALOCUS SEXUAL CONFLICT

Intralocus sexual conflict (IASC) arises when fitness optima for a shared trait differ between the sexes; such conflict may help maintain genetic variation within populations. Sex‐limited expression of sexually antagonistic traits may help resolve the conflict, but the extent of this resolution remains a subject of debate. In species with alternative male reproductive tactics, unresolved conflict should manifest more in a more sexually dimorphic male phenotype. We tested this prediction in the bulb mite (Rhizoglyphus robini), a species in which aggressive fighters coexist with benign scramblers. To do this, we established replicated lines in which we increased the proportion of each of the alternative male morphs using artificial selection. After approximately 40 generations, the proportion of fighters and scramblers stabilized at >0.9 in fighter‐ and scrambler‐selected lines, respectively. We then measured several female fitness components. As predicted by IASC theory, female fecundity and longevity were lower in lines selected for fighters and higher in lines selected for scramblers. This finding indicates that sexually selected phenotypes are associated with an ontogenetic conflict that is not easily resolved. Furthermore, we suggest that IASC may be an important mechanism contributing to the maintenance of genetic variation in the expression of alternative reproductive tactics.     

Sexually selected male weapon is associated with lower inbreeding load but higher sex load in the bulb mite

Elaborate sexually selected ornaments and armaments are costly but increase the reproductive success of their bearers (usually males). It has been postulated that high-quality males can invest disproportionately more in such traits, making those traits honest signals of genetic quality. However, genes associated with such traits may have sexually antagonistic effects on fitness. Here, using a bulb mite Rhizoglyphus robini, a species in which a distinct dimorphism exists between males in the expression of a sexually selected weapon, we compare inbreeding and gender load between lines derived from armed fighters and unarmed scramblers. After four generations of sib-mating, inbreeding depression for female fitness was significantly lower in fighter-derived lines compared to scrambler-derived lines, suggesting that fighter males had significantly higher genetic quality. However, outbred females from fighter-derived lines had significantly lower fitness compared to outbred females from scrambler-derived lines, demonstrating significant gender load associated with the presence of a sexually selected male weapon. Our results imply that under outbreeding, genetic benefits of mating with bearers of elaborate sexually selected traits might be swamped by the costs of decreased fitness of female progeny due to sexually antagonistic effects.     

PATERNAL EFFECTS ON THE EXPRESSION OF A MALE POLYPHENISM

Polyphenic traits are widespread, but compared to other traits, relatively few studies have explored the mechanisms that influence their inheritance. Here we investigated the relative importance of additive, nonadditive genetic, and parental sources of variation in the expression of polyphenic male dimorphism in the mite Rhizoglyphus echinopus, a species in which males are either fighters or scramblers. We established eight inbred lines through eight generations of full‐sibling matings, and then crossed the inbred lines in a partial diallel design. Nymphs were isolated and raised to adulthood with ad libitum food. At adulthood, male morph was recorded for all male offspring. Using a Cockerham–Weir model, we found strong paternal effects for this polyphenic trait that could be either linked to the Y chromosome of males or an indirect genetic effect that is environmentally transmitted. In additional analyses, we were able to corroborate the paternal effects but also detected significant additive effects questioning the Cockerham–Weir analysis. This study reveals the potential importance of paternal effects on the expression of polyphenic traits and sheds light on the complex genetic architecture of these traits.     

Evolution of sexual systems, dispersal strategies and habitat selection in the liverwort genus Radula

? Shifts in sexual systems are among the most common and important transitions in plants and are correlated with a suite of life-history traits. The evolution of sexual systems and their relationships to gametophyte size, sexual and asexual reproduction, and epiphytism are examined here in the liverwort genus Radula. ? The sequence of trait acquisition and the phylogenetic correlations between those traits was investigated using comparative methods. ? Shifts in sexual systems recurrently occurred from dioecy to monoecy within facultative epiphyte lineages. Production of specialized asexual gemmae was correlated to neither dioecy nor strict epiphytism. ? The significant correlations among life-history traits related to sexual systems and habitat conditions suggest the existence of evolutionary trade-offs. Obligate epiphytes do not produce gemmae more frequently than facultative epiphytes and disperse by whole gametophyte fragments, presumably to avoid the sensitive protonemal stage in a habitat prone to rapid changes in moisture availability. As dispersal ranges correlate with diaspore size, this reinforces the notion that epiphytes experience strong dispersal limitations. Our results thus provide the evolutionary complement to metapopulation, metacommunity and experimental studies demonstrating trade-offs between dispersal distance, establishment ability, and life-history strategy, which may be central to the evolution of reproductive strategies in bryophytes.     

Dispersal and life history strategies in epiphyte metacommunities: alternative solutions to survival in patchy,dynamic landscapes

Host trees for obligate epiphytes are dynamic patches that emerge, grow and fall, and metacommunity diversity critically depends on efficient dispersal. Even though species that disperse by large asexual diaspores are strongly dispersal limited, asexual dispersal is common. The stronger dispersal limitation of asexually reproducing species compared to species reproducing sexually via small spores may be compensated by higher growth rates, lower sensitivity to habitat conditions, higher competitive ability or younger reproductive age. We compared growth and reproduction of different groups of epiphytic bryophytes with contrasting dispersal (asexual vs. sexual) and life history strategies (colonists, short- and long-lived shuttle species, perennial stayers) in an old-growth forest stand in the boreo-nemoral region in eastern Sweden. No differences were seen in relative growth rates between asexual and sexual species. Long-lived shuttles had lower growth rates than colonists and perennial stayers. Most groups grew best at intermediate bark pH. Interactions with other epiphytes had a small, often positive effect on growth. Neither differences in sensitivity of growth to habitat conditions nor differences in competitive abilities among species groups were found. Habitat conditions, however, influenced the production of sporophytes, but not of asexual diaspores. Presence of sporophytes negatively affected growth, whereas presence of asexual diaspores did not. Sexual species had to reach a certain colony size before starting to reproduce, whereas no such threshold existed for asexual reproduction. The results indicate that the epiphyte metacommunity is structured by two main trade-offs: dispersal distance vs. reproductive age, and dispersal distance vs. sensitivity to habitat quality. There seems to be a trade-off between growth and sexual reproduction, but not asexual. Trade-offs in species traits may be shaped by conflicting selection pressures imposed by habitat turnover and connectivity rather than by species interactions. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The effect of diet quality and wing morph on male and female reproductive investment in a nuptial feeding ground cricket

A common approach in the study of life-history trade-off evolution is to manipulate the nutrient content of diets during the life of an individual in order observe how the acquisition of resources influences the relationship between reproduction, lifespan and other life-history parameters such as dispersal. Here, we manipulate the quality of diet that replicate laboratory populations received as a thorough test of how diet quality influences the life-history trade-offs associated with reproductive investment in a nuptial feeding Australian ground cricket (Pteronemobius sp.). In this species, both males and females make significant contributions to the production of offspring, as males provide a nuptial gift by allowing females to chew on a modified tibial spur during copulation and feed directing on their haemolymph. Individuals also have two distinct wing morphs, a short-winged flightless morph and a long-winged morph that has the ability to disperse. By manipulating the quality of diet over seven generations, we found that the reproductive investment of males and females were affected differently by the diet quality treatment and wing morph of the individual. We discuss the broader implications of these findings including the differences in how males and females balance current and future reproductive effort in nuptial feeding insects, the changing nature of sexual selection when diets vary, and how the life-history trade-offs associated with the ability to disperse are expected to differ among populations.     

THE EVOLUTION OF ALTERNATIVE REPRODUCTIVE TACTICS IN MALE CARDIOCONDYLA ANTS

Alternative reproductive tactics are often associated with discontinuous variation in morphology but may evolve independent from each other. Based on life‐history data and a phylogeny we examine how male morphology and reproductive behavior are linked in the evolution of the ant genus Cardiocondyla. Wingless Cardiocondyla males engage in lethal fighting for access to female sexuals, whereas winged males disperse and mate away from the nest. This basic pattern shows considerable variation across species. A phylogeny based on ～3 kbp sequence data shows that male diphenism and lethal fighting are ancestral traits tightly linked in evolution. Winged males were lost convergently in several species groups, apparently in response to the low probability of encountering female sexuals in nests without a resident fighter male. An early dichotomy separates two clades with alternative male morphologies and fighting behavior, but phenotype and fighting strategy are not correlated with the presence of winged males.     

Getting the Right Traits: Reproductive and Dispersal Characteristics Predict the Invasiveness of Herbaceous Plant Species

To better understand the effect of species traits on plant invasion, we collected comparative data on 20 reproductive and dispersal traits of 93 herbaceous alien species in the Czech Republic, central Europe, introduced after 1500 A. D. We explain plant invasion success, expressed by two measures: invasiveness, i.e. whether the species is naturalized but non-invasive, or invasive; and dominance in plant communities expressed as the mean cover in vegetation plots. We also tested how important reproductive and dispersal traits are in models including other characteristics generally known to predict invasion outcome, such as plant height, life history and residence time. By using regression/classification trees we show that the biological traits affect invasion success at all life stages, from reproduction (seed production) to dispersal (propagule properties), and the ability to compete with resident species (height). By including species traits information not usually available in multispecies analyses, we provide evidence that traits do play important role in determining the outcome of invasion and can be used to distinguish between alien species that reach the final stage of the invasion process and dominate the local communities from those that do not. No effect of taxonomy ascertained in regression and classification trees indicates that the role of traits in invasiveness should be assessed primarily at the species level.     

Age‐specific oxidative status and the expression of pre‐ and postcopulatory sexually selected traits in male red junglefowl, Gallus gallus

Oxidative stress is emerging as a key factor underpinning life history and the expression of sexually selected traits. Resolving the role of oxidative stress in life history and sexual selection requires a pluralistic approach, which investigates how age affects the relationship between oxidative status (i.e., antioxidants and oxidative damage) and the multiple traits contributing to variation in reproductive success. Here, we investigate the relationship between oxidative status and the expression of multiple sexually selected traits in two‐age classes of male red junglefowl, Gallus gallus, a species which displays marked male reproductive senescence. We found that, irrespective of male age, both male social status and comb size were strongly associated with plasma oxidative status, and there was a nonsignificant tendency for sperm motility to be associated with seminal oxidative status. Importantly, however, patterns of plasma and seminal antioxidant levels differed markedly in young and old males. While seminal antioxidants increased with plasma antioxidants in young males, the level of seminal antioxidants remained low and was independent of plasma levels in old males. In addition, old males also accumulated more oxidative damage in their sperm DNA. These results suggest that antioxidant allocation across different reproductive traits and somatic maintenance might change drastically as males age, leading to age‐specific patterns of antioxidant investment.     

Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.     

Life‐history syndromes: Integrating dispersal through space and time

Recent research has highlighted interdependencies between dispersal and other life‐history traits, i.e. dispersal syndromes, thereby revealing constraints on the evolution of dispersal and opportunities for improved ability to predict dispersal by considering suites of dispersal‐related traits. This review adds to the growing list of life‐history traits linked to spatial dispersal by emphasising the interdependence between dispersal through space and time, i.e. life‐history diversity that distributes individuals into separate reproductive events. We reviewed the literature that has simultaneously investigated spatial and temporal dispersal to examine the prediction that traits of these two dispersal strategies are negatively correlated. Our results suggest that negative covariation is widely anticipated from theory. Empirical studies often reported evidence of weak negative covariation, although more complicated patterns were also evident, including across levels of biological organisation. Existing literature has largely focused on plants with dormancy capability, one or two phases of the dispersal process (emigration and/or transfer) and a single level of biological organisation (theory: individual; empirical: species). We highlight patterns of covariation across levels of organisation and conclude with a discussion of the consequences of dispersal through space and time and future research areas that should improve our understanding of dispersal‐related life‐history syndromes.     

Structural complexity of the environment affects the survival of alternative male reproductive tactics

Alternative reproductive tactics in males are often associated with divergent phenotypes expressed as phenotypically plastic threshold traits. The evolution of threshold traits in these species has been modeled under the conditional evolutionarily stable strategy (ESS). Both strategic and genetic models predict that perturbations to the fitness trade-off between the male morphs will lead to a shift in the ESS switch point of the threshold. So far, demographic factors that influence the competitive ability of male morphs have been investigated and related to intraspecific population variation in male dimorphic thresholds. Here we reveal evidence for the theoretical prediction that abiotic features of the environment, in particular its structural complexity, are likely to influence the ESS threshold. In the male dimorphic mite Sancassania berlesei, we monitored the survival of aggressive fighter males and their benign scrambler counterparts in populations that differed in structural complexity. We found that, consistent with our prediction, the complex habitat favored fighter males, enabling them to kill a greater number of rival scramblers. We found no effect of habitat complexity on the survival of fighter males. These results demonstrate how abiotic as well as biotic aspects of the environment can be important in determining the frequencies of males adopting alternative tactics in different species or populations.     

Experimental evolution reveals balancing selection underlying coexistence of alternative male reproductive phenotypes

Heritable alternative reproductive phenotypes (ARPs), which differ in traits associated with competition for mates, occur across taxa. If polymorphism in the genes underlying ARPs is maintained by balancing selection, selection should return ARP proportions to their equilibrium if that equilibrium is perturbed. Here, we used an experimental evolution approach to directly test this prediction in male Rhizoglyphus robini, in which two heritable morphs occur: armored fighters and more female‐like, benign scramblers. Using selection lines nearly fixed for male morph, we constructed replicate populations consisting of 50% or 94% fighters, and allowed them to evolve for 14 generations in two types of environment: simple or spatially complex. We found that in both types of populations, the proportion of fighters converged on values within a narrow range of 0.70–0.83, although the rate of convergence was slower in the complex environment. Our results thus demonstrate balancing selection acting on polymorphism(s) underlying ARPs.     

Sex- and age-dependent effects of population density on life history traits of red deer Cervus elaphus in a temperate forest

We studied both the short‐ and long‐term effects of density on three life history traits of a red deer population inhabiting a temperate forest. Both male and female body mass increased when population density decreased, but male mass changed to a greater extent than female mass. Density did not influence female survival irrespective of age, however, survival of males was lower at high density for all age classes except the prime‐age class. Pregnancy rates of primiparous females increased markedly with decreasing density, whereas those of adult hinds were fairly constant and unrelated to density. For both sexes, of the studied life history traits we detected a long‐term effect of density at birth (cohort effect) only on body mass. These results suggest that density influences life history traits in the same way as factors of environmental variation such as climate. In this population we did not find any evidence for an influence of climatic conditions on life history traits of red deer. Both mild winters and the absence of summer droughts during the study period could account for such an absence of climatic effects. We interpreted our results to show that 1) as expected for a highly dimorphic and polygynous species such as red deer, male traits showed consistently higher sensitivity to variation in density than female traits, illustrating possible costs caused by sexual selection in males, 2) the female‐based Eberhardt's model according to which increasing density should sequentially affect juvenile survival, reproductive rates of primiparous females, reproductive rates of adults and lastly adult survival was only partly supported because we found that pregnancy rate of primiparous females rather than juvenile survival was the most sensitive trait to variation in density. We propose that including variation in male traits would improve the accuracy of models of population dynamics of large mammals, at least for highly dimorphic species. Because the population we studied was not fenced, we only measured apparent survival. We discuss how dispersal, in relation to the phenotypic quality of young deer, might be a potential regulating factor under such conditions.     

Nutrient‐dependent allometric plasticity in a male‐diphenic mite

Male secondary sexual traits often scale allometrically with body size. These allometries can be variable within species and may shift depending on environmental conditions, such as food quality. Such allometric plasticity has been hypothesized to initiate local adaptation and evolutionary diversification of scaling relationships, but is under‐recorded, and its eco‐evolutionary effects are not well understood. Here, we tested for allometric plasticity in the bulb mite (Rhizoglyphus robini), in which large males tend to develop as armed adult fighters with thickened third legs, while small males become adult scramblers without thickened legs. We first examined the ontogenetic timing for size‐ and growth‐dependent male morph determination, using experimentally amplified fluctuations in growth rate throughout juvenile development. Having established that somatic growth and body size determine male morph expression immediately before metamorphosis, we examined whether the relationship between adult male morph and size at metamorphosis shifts with food quality. We found that the threshold body size for male morph expression shifts toward lower values with deteriorating food quality, confirming food‐dependent allometric plasticity. Such allometric plasticity may allow populations to track prevailing nutritional conditions, potentially facilitating rapid evolution of allometric scaling relationships.     

Using Age-Based Life History Data to Investigate the Life Cycle and Vulnerability of Octopus cyanea

Octopus cyanea is taken as an unregulated, recreationally fished species from the intertidal reefs of Ningaloo, Western Australia. Yet despite its exploitation and importance in many artisanal fisheries throughout the world, little is known about its life history, ecology and vulnerability. We used stylet increment analysis to age a wild O. cyanea population for the first time and gonad histology to examine their reproductive characteristics. O. cyanea conforms to many cephalopod life history generalisations having rapid, non-asymptotic growth, a short life-span and high levels of mortality. Males were found to mature at much younger ages and sizes than females with reproductive activity concentrated in the spring and summer months. The female dominated sex-ratios in association with female brooding behaviours also suggest that larger conspicuous females may be more prone to capture and suggests that this intertidal octopus population has the potential to be negatively impacted in an unregulated fishery. Size at age and maturity comparisons between our temperate bordering population and lower latitude Tanzanian and Hawaiian populations indicated stark differences in growth rates that correlate with water temperatures. The variability in life history traits between global populations suggests that management of O. cyanea populations should be tailored to each unique set of life history characteristics and that stylet increment analysis may provide the integrity needed to accurately assess this.     

Increased lifetime reproductive success for Siberian jay (Perisoreus infaustus) males with delayed dispersal

In a crowded environment the natal territory could serve as a haven for young and inexperienced offspring until a breeding vacancy emerges. Delayed dispersal and association with kin could then offer adaptive benefits through an individual fitness gain. Here we report that delayed dispersal is associated with a higher lifetime individual fitness in Siberian jay (Perisoreus infaustus) males. Sons bred more successfully and had more reproductive events in life when they delayed dispersal. The higher lifetime reproductive success when sons disperse later in life is sufficient to promote postponement of natal dispersal, suggesting that dispersal is delayed due to ecological constraints on access to high-quality habitats. We argue that the maintenance of this variation in the timing of dispersal and reproductive success can be reconciled with non-genetic mechanisms driving dispersal. Social dominance within broods reflecting environmental conditions during growth is such a mechanism.