Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes

Abbreviations of the complex life cycle of trematodes, from three to two hosts, have occurred repeatedly and independently among trematode lineages. This is usually facultative and achieved via progenesis: following encystment in the second intermediate host, the metacercaria develops precociously into an egg-producing adult, bypassing the need to reach a definitive host. Given that it provides relatively cheap insurance against a shortage of definitive hosts, it is not clear why facultative progenesis has only evolved in a few taxa. Here a comparative approach is used to test whether progenetic trematodes are characterized by larger body size and egg volumes, two traits that correlate with other key life history features, than other trematodes. These traits may constrain the evolution of progenesis, because precocious maturation might be impossible when the size difference between the metacercaria and a reproductive adult is too large. First, trematode species belonging to genera in which progenesis has been documented were found not to differ significantly from other trematode species. Second, using within-genus paired comparisons across 19 genera in which progenesis has been reported, progenetic species did not differ, with respect to body size or egg size, from their non-progenetic congeners. Third, using intraspecific paired comparisons in species where progenesis is facultative, no difference was observed in the sizes of eggs produced by worms in both the intermediate and definitive host, suggesting that opting for progenesis does not influence the size of a worm's eggs. Overall, the lack of obvious differences in body or egg size between trematodes with truncated life cycles and those with the normal three-host cycle indicates that basic life history characteristics are not acting as constraints on the evolution of progenesis; trematodes of all sizes can do it. Why facultative progenesis is not more widespread remains a mystery.     

Sex‐specific selection under environmental stress in seed beetles

Sexual selection can increase rates of adaptation by imposing strong selection in males, thereby allowing efficient purging of the mutation load on population fitness at a low demographic cost. Indeed, sexual selection tends to be male‐biased throughout the animal kingdom, but little empirical work has explored the ecological sensitivity of this sex difference. In this study, we generated theoretical predictions of sex‐specific strengths of selection, environmental sensitivities and genotype‐by‐environment interactions and tested them in seed beetles by manipulating either larval host plant or rearing temperature. Using fourteen isofemale lines, we measured sex‐specific reductions in fitness components, genotype‐by‐environment interactions and the strength of selection (variance in fitness) in the juvenile and adult stage. As predicted, variance in fitness increased with stress, was consistently greater in males than females for adult reproductive success (implying strong sexual selection), but was similar in the sexes in terms of juvenile survival across all levels of stress. Although genetic variance in fitness increased in magnitude under severe stress, heritability decreased and particularly so in males. Moreover, genotype‐by‐environment interactions for fitness were common but specific to the type of stress, sex and life stage, suggesting that new environments may change the relative alignment and strength of selection in males and females. Our study thus exemplifies how environmental stress can influence the relative forces of natural and sexual selection, as well as concomitant changes in genetic variance in fitness, which are predicted to have consequences for rates of adaptation in sexual populations.     

Life cycle truncation in a trematode: does higher temperature indicate shorter host longevity?

The typical three-host life cycle of most trematodes creates transmission challenges for which a variety of adaptations have evolved to increase the probability of transmission. Some species can abbreviate their life cycle via progenesis, the precocious maturation of the parasite in the second intermediate host resulting in the production of eggs through self-fertilisation without requiring a definitive host. Adoption of the progenetic life cycle may be a conditional strategy in response to different environmental cues related to low probability of transmission to the definitive host. Using high water temperature and/or limited diet as experimental stressors, we tested the effect of body condition and life span of the fish second intermediate host on facultative truncation of the typical three-host life cycle by progenesis in Stegodexamene anguillae. The results suggest that environmental cues, such as temperature and encystment site, may signal transmission opportunities to the parasite so that it may adjust its developmental strategy accordingly. Indeed, a greater proportion of worms became progenetic at higher temperatures, and progenesis was more common among worms encysted in the gonads or body cavity of their fish hosts than among those in other host tissues. These findings highlight the often unrecognised plasticity in parasite developmental and transmission strategies.     

Geographic variation in life cycle strategies of a progenetic trematode

Numerous parasite species have evolved complex life cycles with multiple, subsequent hosts. In trematodes, each transmission event in multi-host life cycles selects for various adaptations, one of which is facultative life cycle abbreviation. This typically occurs through progenesis, i.e., precocious maturity and reproduction via self-fertilization within the second intermediate host. Progenesis eliminates the need for the definitive host and facilitates life cycle completion. Adopting a progenetic cycle may be a conditional strategy in response to environmental cues related to low probability of transmission to the definitive host. Here, the effects of environmental factors on the reproductive strategy of the progenetic trematode Stegodexamene anguillae were investigated using comparisons among populations. In the 3-host life cycle, S. anguillae sexually reproduces within eel definitive hosts, whereas in the progenetic life cycle, S. anguillae reproduces by selfing within the metacercaria cyst in tissues of small fish intermediate hosts. Geographic variation was found in the frequency of progenesis, independent of eel abundance. Progenesis was affected by abundance and length of the second intermediate fish host as well as encystment site within the host. The present study is the first to compare life cycle strategies among parasite populations, providing insight into the often unrecognized plasticity in parasite developmental strategies and transmission.     

Field evidence challenges the often‐presumed relationship between early male maturation and female‐biased sexual size dimorphism

Female‐biased sexual size dimorphism (SSD) is often considered an epiphenomenon of selection for the increased mating opportunities provided by early male maturation (i.e., protandry). Empirical evidence of the adaptive significance of protandry remains nonetheless fairly scarce. We use field data collected throughout the reproductive season of an SSD crab spider, Mecaphesa celer, to test two hypotheses: Protandry provides fitness benefits to males, leading to female‐biased SSD, or protandry is an indirect consequence of selection for small male size/large female size. Using field‐collected data, we modeled the probability of mating success for females and males according to their timing of maturation. We found that males matured earlier than females and the proportion of virgin females decreased abruptly early in the season, but unexpectedly increased afterward. Timing of female maturation was not related to clutch size, but large females tended to have more offspring than small females. Timing of female and male maturation was inversely related to size at adulthood, as early‐maturing individuals were larger than late‐maturing ones, suggesting that both sexes exhibit some plasticity in their developmental trajectories. Such plasticity indicates that protandry could co‐occur with any degree and direction of SSD. Our calculation of the probability of mating success along the season shows multiple male maturation time points with similar predicted mating success. This suggests that males follow multiple strategies with equal success, trading‐off access to virgin females with intensity of male–male competition. Our results challenge classic hypotheses linking protandry and female‐biased SSD, and emphasize the importance of directly testing the often‐assumed relationships between co‐occurring animal traits.     

Sex‐specific plasticity and genotype × sex interactions for age and size of maturity in the sheepshead swordtail,Xiphophorus birchmanni

Responses to sexually antagonistic selection are thought to be constrained by the shared genetic architecture of homologous male and female traits. Accordingly, adaptive sexual dimorphism depends on mechanisms such as genotype‐by‐sex interaction (G×S) and sex‐specific plasticity to alleviate this constraint. We tested these mechanisms in a population of Xiphophorus birchmanni (sheepshead swordtail), where the intensity of male competition is expected to mediate intersexual conflict over age and size at maturity. Combining quantitative genetics with density manipulations and analysis of sex ratio variation, we confirm that maturation traits are dimorphic and heritable, but also subject to large G×S. Although cross‐sex genetic correlations are close to zero, suggesting sex‐linked genes with important effects on growth and maturation are likely segregating in this population, we found less evidence of sex‐specific adaptive plasticity. At high density, there was a weak trend towards later and smaller maturation in both sexes. Effects of sex ratio were stronger and putatively adaptive in males but not in females. Males delay maturation in the presence of mature rivals, resulting in larger adult size with subsequent benefit to competitive ability. However, females also delay maturation in male‐biased groups, incurring a loss of reproductive lifespan without apparent benefit. Thus, in highly competitive environments, female fitness may be limited by the lack of sex‐specific plasticity. More generally, assuming that selection does act antagonistically on male and female maturation traits in the wild, our results demonstrate that genetic architecture of homologous traits can ease a major constraint on the evolution of adaptive dimorphism.     

Sexual selection on spontaneous mutations strengthens the between‐sex genetic correlation for fitness

A proposed benefit to sexual selection is that it promotes purging of deleterious mutations from populations. For this benefit to be realized, sexual selection, which is usually stronger on males, must purge mutations deleterious to both sexes. Here, we experimentally test the hypothesis that sexual selection on males purges deleterious mutations that affect both male and female fitness. We measured male and female fitness in two panels of spontaneous mutation‐accumulation lines of the fly, Drosophila serrata, each established from a common ancestor. One panel of mutation accumulation lines limited both natural and sexual selection (LS lines), whereas the other panel limited natural selection, but allowed sexual selection to operate (SS lines). Although mutation accumulation caused a significant reduction in male and female fitness in both the LS and SS lines, sexual selection had no detectable effect on the extent of the fitness reduction. Similarly, despite evidence of mutational variance for fitness in males and females of both treatments, sexual selection had no significant impact on the amount of mutational genetic variance for fitness. However, sexual selection did reshape the between‐sex correlation for fitness: significantly strengthening it in the SS lines. After 25 generations, the between‐sex correlation for fitness was positive but considerably less than one in the LS lines, suggesting that, although most mutations had sexually concordant fitness effects, sex‐limited, and/or sex‐biased mutations contributed substantially to the mutational variance. In the SS lines this correlation was strong and could not be distinguished from unity. Individual‐based simulations that mimick the experimental setup reveal two conditions that may drive our results: (1) a modest‐to‐large fraction of mutations have sex‐limited (or highly sex‐biased) fitness effects, and (2) the average fitness effect of sex‐limited mutations is larger than the average fitness effect of mutations that affect both sexes similarly.     

Facultative paedomorphosis as a mechanism promoting intraspecific niche differentiation

Organisms with complex life cycles are characterized by a metamorphosis that allows for a major habitat shift and the exploitation of alternative resources. However, metamorphosis can be bypassed in some species through a process called paedomorphosis, resulting in the retention of larval traits at the adult stage and is considered important at both micro‐ and macroevolutionary scales. In facultatively paedomorphic populations of newts, some individuals retain gills and a fully aquatic life at the adult stage (paedomorphs), while others undergo complete metamorphosis (metamorphs), allowing for a terrestrial life‐stage. Because facultative paedomorphosis affects trophic structures and feeding mechanism of newts, one hypothesis is that it may be maintained as a trophic polymorphism, with the advantage to lessen intraspecific competition during the shared aquatic life‐stage. Here, we tested this hypothesis combining stomach content data with stable isotope techniques, using carbon and nitrogen stable isotopes, in facultatively paedomorphic alpine newts Ichthyosaura alpestris. Both stomach content and stable isotope analyses showed that paedomorphs had smaller trophic niches and were more reliant on pelagic resources, while metamorphs relied more on littoral resources, corresponding to a polyphenism along the littoral–pelagic axis and the extension of the population's trophic niche to otherwise ‘underused’ pelagic resources by paedomorphs. Interestingly, stable isotopes revealed that the trophic polyphenism was less marked in males than in females and potentially linked to sexual activity. Although paedomorphosis and metamorphosis are primarily seen as results of tradeoffs between the advantages of using aquatic versus terrestrial habitats, this study provides evidence that additional forces, such as intraspecific trophic niche differences between morphs and trophic niche expansion, may play an important role in the persistence of this dimorphism in heterogeneous environments. Moreover, the different patterns found in males and females show the importance of considering sex to understand the evolutionary ecology of trophic polymorphisms.     

Time spent in distinct life history stages has sex‐specific effects on reproductive fitness in wild Atlantic salmon

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a 4‐year pedigree to investigate if time spent in two distinct life history stages has sex‐specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW, measured in years), and years spent in the marine environment as adults (sea age, SW, measured in sea winters) on 264 sexually mature adults collected on a river spawning ground. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5,000 offspring). Sea age is significantly and positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: 62.2% increase in offspring/SW and 34.8% increase in mate number/SW; males: 201.9% offspring/SW and 60.3% mates/SW). Younger freshwater age was significantly related to older sea age and thus increased reproductive fitness, but only among females (females: ?33.9% offspring/FW and ?32.4% mates/FW). This result implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and more males returned at a younger age than females despite the reproductive fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex‐specific consequence on female reproductive fitness, demonstrating a life history trade‐off between maturation and reproduction in wild Atlantic salmon.     

Morph switching in a dimorphic population of <Emphasis Type="Italic">Triturus alpestris</Emphasis> (Amphibia,Caudata)

The usual life cycle of Alpine newts comprises an aquatic larval stage and a terrestrial juvenile and adult stage. However, some populations differ from this pattern in exhibiting facultative paedomorphosis where some individuals reach sexual maturity while retaining larval traits such as gills and gill slits. While paedomorphic newts can, in some circumstances, initiate metamorphosis, once a newt has commenced metamorphosis, the state is irreversible. Because the frequency of this switching from one morph to the other has never been quantified in the wild, we attempted to estimate switching rate and survival by carrying out a 3-year monitoring survey of a population inhabiting an alpine lake. While morph switching did occur in this population, it involved a relatively low proportion of the paedomorphs (approx. 12%), suggesting that metamorphosis is not favoured in the study population. The hypothesis of paedomorphic advantage was not supported since neither survival nor body condition differed between morphs. The ontogenetic pathway of wild Alpine newts is thus characterised by two forks in the developmental pathway. The first occurs during the larval stage (metamorphosis vs. paedomorphosis), and the second occurs in paedomorphic adults (switching for metamorphosis vs. continuation of the paedomorphic lifestyle). Such a two-level decision process may allow individuals to cope with environmental uncertainty.     

Facultative and non‐facultative sex ratio adjustments in a dimorphic bird species

If parental allocation to each offspring sex has the same cost/benefit ratio, Fisher's hypothesis predicts a sex ratio biased towards the cheaper sex. However, in dimorphic birds there is little evidence for this, especially at hatching. We investigated the pre‐fledgling 1) sex ratio, 2) body condition and 3) sex‐differential mortality in a population of the glossy ibis Plegadis falcinellus, in southern Spain between 2001 and 2011. We defined two age groups for the period between hatching and fledging. We also compared pre‐fledgling with the autumn sex ratio. Metabolic rates were estimated by the doubly labeled water (DLW) technique to establish that sons (the bigger sex) were 18% more energy demanding than daughters, and to compute the predicted Fisher's sex ratio (0.465). As population size increased between years, body condition decreased in both sexes, and mortality increased more for daughters than sons prior to fledging. At the same time, the proportion of males among chicks close to fledging increased (average sex ratio: 0.606) while the proportion close to hatching decreased (average sex ratio: 0.434, in line with Fisher's prediction). Furthermore, the proportions of males at fledging and the following autumn were negatively correlated across years. We suggest that, as population density increased and conditions worsened the larger sex had relatively higher survival. These differences in survival produce a shift from a facultative female‐biased sex ratio at hatching into a non‐facultative male‐biased sex ratio of fledglings. Additionally, the excess of males at fledging was counterbalanced by sex‐related dispersal during the autumn. Overall, glossy ibis sex ratio is a product of a combination of facultative and non‐facultative adjustments triggered by environmental conditions, driven by rapid population growth, and mediated by highly interrelated life‐history traits such as body condition, mortality, and dispersal.     

RAPID LOSS OF BEHAVIORAL PLASTICITY AND IMMUNOCOMPETENCE UNDER INTENSE SEXUAL SELECTION

Phenotypic plasticity allows animals to maximize fitness by conditionally expressing the phenotype best adapted to their environment. Although evidence for such adjustment in reproductive tactics is common, little is known about how phenotypic plasticity evolves in response to sexual selection. We examined the effect of sexual selection intensity on phenotypic plasticity in mating behavior using the beetle Callosobruchus maculatus. Male genital spines harm females during mating and females exhibit copulatory kicking, an apparent resistance trait aimed to dislodge mating males. After exposing individuals from male‐ and female‐biased experimental evolution lines to male‐ and female‐biased sociosexual environments, we examined behavioral plasticity in matings with standard partners. While females from female‐biased lines kicked sooner after exposure to male‐biased sociosexual contexts, in male‐biased lines this plasticity was lost. Ejaculate size did not diverge in response to selection history, but males from both treatments exhibited plasticity consistent with sperm competition intensity models, reducing size as the number of competitors increased. Analysis of immunocompetence revealed reduced immunity in both sexes in male‐biased lines, pointing to increased reproductive costs under high sexual selection. These results highlight how male and female reproductive strategies are shaped by interactions between phenotypically plastic and genetic mechanisms of sexual trait expression.     

Progenesis and facultative life cycle abbreviation in trematode parasites: Are there more constraints than costs?

Complex life cycles provide advantages to parasites (longer life span, higher fecundity, etc.), but also represent a series of unlikely events for which many adaptations have evolved (asexual multiplication, host finding mechanisms, etc.). Some parasites use a radical strategy where the definitive host is dropped; life cycle abbreviation is most often achieved through progenesis (i.e. early maturation) and reproduction in the second intermediate host. In many progenetic species, both the typical and abbreviated life cycles are maintained. However, conditions that trigger the adoption of one or the other strategy, and the pros and cons of each parasite life history strategy, are often complex and poorly understood. We used experimental infections with the trematode Coitocaecum parvum in its fish definitive host to test for potential costs of progenesis in terms of lifespan and fecundity. We show that individuals that adopt progenesis in the intermediate host are still able to establish in the definitive host and achieve higher survival and fecundity than conspecifics adopting the typical three-host life cycle. Our results and that of previous studies show that there seems to be few short-term costs associated with progenesis in C. parvum. Potential costs of self-fertilization and inbreeding are often suggested to select for the maintenance of both life-history strategies in species capable of facultative progenesis. We suggest that, at least for our focal species, there are more constraints than costs limiting its adoption. Progenesis and the abbreviated cycle may become the typical life-history strategy while reproduction in the vertebrate definitive host is now a secondary alternative when progenesis is impossible (e.g. limited host resources, etc.). Whether this pattern can be generalized to other progenetic trematodes is unknown and would require further studies.     

The contribution of the mitochondrial genome to sex‐specific fitness variance

Maternal inheritance of mitochondrial DNA (mtDNA) facilitates the evolutionary accumulation of mutations with sex‐biased fitness effects. Whereas maternal inheritance closely aligns mtDNA evolution with natural selection in females, it makes it indifferent to evolutionary changes that exclusively benefit males. The constrained response of mtDNA to selection in males can lead to asymmetries in the relative contributions of mitochondrial genes to female versus male fitness variation. Here, we examine the impact of genetic drift and the distribution of fitness effects (DFE) among mutations—including the correlation of mutant fitness effects between the sexes—on mitochondrial genetic variation for fitness. We show how drift, genetic correlations, and skewness of the DFE determine the relative contributions of mitochondrial genes to male versus female fitness variance. When mutant fitness effects are weakly correlated between the sexes, and the effective population size is large, mitochondrial genes should contribute much more to male than to female fitness variance. In contrast, high fitness correlations and small population sizes tend to equalize the contributions of mitochondrial genes to female versus male variance. We discuss implications of these results for the evolution of mitochondrial genome diversity and the genetic architecture of female and male fitness.     

Sex ratio at mating does not modulate age fitness effects in Drosophila melanogaster

Understanding the effects of male and female age on reproductive success is vital to explain the evolution of life history traits and sex‐specific aging. A general prediction is that pre‐/postmeiotic aging processes will lead to a decline in the pre‐ and postcopulatory abilities of both males and females. However, in as much the sexes have different strategies to optimize their fitness, the decline of reproductive success late in life can be modulated by social context, such as sex ratio, in a sex‐specific manner. In this study, we used Drosophila melanogaster to investigate whether sex ratio at mating modulates age effects on male and female reproductive success. As expected, male and female age caused a decrease in reproductive success across male‐biased and female‐biased social contexts but, contrary to previous findings, social context did not modulate age‐related fitness decline in either of the two sexes. We discuss these results in the light of how sex ratio might modulate pre‐/postcopulatory abilities and the opportunity for inter‐ and intrasexual competition in D. melanogaster, and generally suggest that social context effects on these processes are likely to be species specific.     

MALE‐BIASED FITNESS EFFECTS OF SPONTANEOUS MUTATIONS IN DROSOPHILA MELANOGASTER

In populations with males and females, sexual selection may often represent a major component of overall selection. Sexual selection could act to eliminate deleterious alleles in concert with other forms of selection, thereby improving the fitness of sexual populations. Alternatively, the divergent reproductive strategies of the sexes could promote the maintenance of sexually antagonistic variation, causing sexual populations to be less fit. The net impact of sexual selection on fitness is not well understood, due in part to limited data on the sex‐specific effects of spontaneous mutations on total fitness. Using a set of mutation accumulation lines of Drosophila melanogaster, we found that mutations were deleterious in both sexes and had larger effects on fitness in males than in females. This pattern is expected to reduce the mutation load of sexual females and promote the maintenance of sexual reproduction.     

Facultative Sex Allocation and Sex‐Specific Offspring Survival in Barrow's Goldeneyes

Sex allocation theory predicts that females should bias their reproductive investment towards the sex generating the greatest fitness returns. The fitness of male offspring is often more dependent upon maternal investment, and therefore, high‐quality mothers should invest in sons. However, the local resource competition hypothesis postulates that when offspring quality is determined by maternal quality or when nest site and maternal quality are related, high‐quality females should invest in the philopatric sex. Waterfowl – showing male‐biased size dimorphism but female‐biased philopatry – are ideal for differentiating between these alternatives. We utilized molecular sexing methods and high‐resolution maternity tests to study the occurrence and fitness consequences of facultative sex allocation in Barrow's goldeneyes (Bucephala islandica). We determined how female structural size, body condition, nest‐site safety and timing of reproduction affected sex allocation and offspring survival. We found that the overall sex ratio was unbiased, but in line with the local resource competition hypothesis, larger females produced female‐biased broods and their broods survived better than those of smaller females. This bias occurred despite male offspring being larger and tending to have lower post‐hatching survival. The species shows strong female breeding territoriality, so the benefit of inheriting maternal quality by philopatric daughters may exceed the potential mating benefit for sons of high‐quality females.     

Sex‐biased transmission of a complex life‐cycle parasite: why males matter

Male‐bias in parasite infection exists in a variety of host–parasite systems, but the epidemiological importance of males and, specifically, whether males are responsible for producing a disproportionate amount of onward transmission events (male‐biased transmission) has seldom been tested. The primary goal of our study was to experimentally test for male‐biased transmission in a system with no sex‐biased prevalence. We performed a longitudinal field experiment and continuously removed intestinal nematode parasites from either male or female white‐footed mice and recorded the subsequent transmission among the untreated sex. We predicted males are responsible for the majority of transmission and female mice would have lower infection prevalence under the male‐anthelmintic treatment than controls and that male mice would experience little or no change in infection prevalence under female‐anthelmintic treatment compared to controls. Our second goal was to evaluate physiological hypotheses relating to the mechanisms that could generate the observed transmission pattern. To that end, we examined a cross‐sectional sample of hosts to explicitly test for differences in parasite intensity, parasite egg shedding rate and reproductive output per parasite between male and female hosts. Removing parasites from male mice resulted in lower infection rates among female mice but, in contrast, there was no effect of female‐deworming on infection rates among male mice; providing evidence that males provide disproportionately greater numbers of transmission events than females. We found no difference in prevalence, intensity, or fecundity of parasites between sexes in the cross‐sectional sample of mice and rejected the mechanistic hypotheses. Without male‐biased prevalence, intensity, or parasite fecundity, we concluded that male‐biased transmission is unlikely to be created via physiological differences and the parsimonious explanation is that male behavior spreads infective stages in a more successful manner. We demonstrate that transmission heterogeneities can exist in the absence of individual heterogeneities in infection.     

Progenesis in dicyemids

Dicyemids (Phylum Dicyemida) are the most common and characteristic endosymbiont living in the renal sac of benthic cephalopod molluscs. Precocious development of a hermaphroditic gonad occurs in the larvae and smaller juveniles of 40 dicyemid species from 17 cephalopod species so far and is the usual phenomenon in dicyemids. Based on the developmental and morphological features of precocious individuals, progenesis (a form of heterochrony) is the appropriate term for such precocious development. In general, progenetic individuals have much lower fecundity than normal ones because of their smaller body size, and therefore, it appears to be a disadvantageous reproductive trait. Nonetheless, the number of progenetic individuals consists of 30%–50% of the population, a relatively large proportion suggesting that the presence of progenetic individuals probably plays an important role in life history strategy. Precocious development significantly reduces growth time and enables early maturation. Progenetic individuals are common in short-living cephalopod species, in which precocious development seems appropriate for dicyemids, enabling fast larval release before the end of the host's life span.     

On the possible role of nonreproductive traits for the evolution of unisexuality: Life‐history variation among males,females, and hermaphrodites in Opuntia robusta (Cactaceae)

In angiosperms, dioecy has arisen in 871–5,000 independent events, distributed in approximately 43% of the flowering families. The reproductive superiority of unisexuals has been the favorite explanation for the evolution of separate sexes. However, in several instances, the observed reproductive performance of unisexuals, if any, does not seem to compensate for the loss of one of the sex functions. The involvement of fitness components not directly associated with reproduction is a plausible hypothesis that has received little attention. Life‐history traits recently recognized as predictors of plant performance were compared among males, females, and hermaphrodites of a rare trioecious Opuntia robusta population in the field, using the cladode as the study unit. Cladode mortality by domestic herbivores was common and higher in females and hermaphrodites than in males. Males, females, or both displayed lower shrinkage and higher rates of survival, growth, and reproductive frequency than hermaphrodites. Unisexuals simultaneously outperformed hermaphrodites in demographic traits known to compete for common limiting resources, such as the acceleration of reproductive maturation (progenesis) and survival. A meta‐analysis combining the outcomes of each of the analyzed life‐history traits revealed a tendency of males (d₊₊ = 1.03) and females (d₊₊ = 0.93) to outperform hermaphrodites in presumably costly demographic options. Clonality is induced by human or domestic animal plant sectioning; and males and females highly exceeded hermaphrodites in their clonality potential by a factor of 8.3 and 5.3, respectively. The performances of unisexuals in the analyzed life‐history traits may enhance their reproductive potential in the long run and their clonality potential and could explain the observed increase of unisexuality in the population. Life‐history traits can be crucial for the evolution of unisexuality, but their impact appears to be habitat specific and may involve broad ontogenetic changes.