Predicting the effects of exploitation on male-first sex-changing fish

Sex change is widespread among tropical marine fishes, many of which are targeted by fisheries. Conservation concerns have been raised that sex-changing species may be particularly prone to overexploitation by size-selective fishing. In the case of male-first sex-changers, populations may become egg limited if large females are disproportionately killed. However, if males reduce the size at which they change sex in response to higher female mortality, the population may still be sufficiently productive. We develop an age-based model to explore the effects of fishing on two types of male-first sex-changing fish: one with flexibility in size-at-sex-change and one without. These effects were compared with those of non-sex-changing populations with similar life-history and population characteristics. The model predicts that if male-first sex-changers cannot respond to elevated female mortality by adjusting their size-at-sex-change, the population will be more prone to recruitment limitation and extinction than non-sex-changers. These effects will be amplified as smaller individuals become susceptible to fishing mortality. However, if size-at-sex-change is flexible, sex-changers may be as resilient to fishing as non-sex-changers. Knowledge of a species' size-at-sex-change, and the mechanisms controlling it, should be fundamental to the selection of fisheries conservation strategies.     

Relative size-at-sex-change in parrotfishes across the Caribbean: is there variance in a supposed life-history invariant?

Invariant life-history theory has been used to identify parallels in life histories across diverse taxa. One important invariant life-history model predicts that, given simple assumptions and conditions, size-at-sex-change relative to maximum attainable body size (relative size-at-sex-change, RSSC) will be invariant across populations and species in sequential hermaphrodites. Even if there are broad species-wide limits to RSSC, populations could fine-tune RSSC to local conditions and, consequently, exhibit subtle but important differences in timing of sex change. Previous analyses of the invariant sex-change model have not explicitly considered the potential for meaningful differences in RSSC within the confines of a broader ‘invariance’. Furthermore, these tests differ in their geographical and taxonomic scope, which could account for their conflicting conclusions. We test the model using several populations of three female-first sex-changing Caribbean parrotfish species. We first test for species-wide invariance using traditional log–log regressions and randomisation analyses of population-specific point estimates of RSSC. We then consider error around these point estimates, which is rarely incorporated into invariant analyses, to test for differences among populations in RSSC. Log–log regressions could not unequivocally diagnose invariance in RSSC across populations; randomisation tests identified an invariant RSSC in redband parrotfish only. Analyses that incorporated within-population variability in RSSC revealed differences among populations in timing of sex change, which were independent of geography for all species. While RSSC may be evolutionarily constrained (as in redband parrotfish), within these bounds the timing of sex change may vary among populations. This variability is overlooked by traditional invariant analyses and not predicted by the existing invariant model.     

Anthropogenic harvesting pressure and changes in life history: insights from a rocky intertidal limpet

The importance of large breeding individuals for maintaining the health of marine fish and invertebrate populations has long been recognized. Unfortunately, decades of human harvesting that preferentially remove larger individuals have led to drastic reductions in body sizes of many of these species. Such size-selective harvesting is particularly worrisome for sequentially hermaphroditic species where the larger size classes are composed primarily of one sex. Whether these species can maintain stable sex ratios under sustained harvesting pressure depends on the level of plasticity of their life-history traits. Here, we show that populations of a marine limpet (Lottia gigantea) can adjust a fundamental aspect of their life history (the timing of sex change) when subjected to size-selective harvesting. As predicted by theoretical models, individuals from harvested populations change sex at smaller sizes and grow at slower rates compared to individuals from protected populations. In addition, the relative size at which the change from male to female occurs remains constant (~0.75; size at sex change/maximum size) across populations, regardless of harvesting pressure. Our results show that population-level demographic and life-history data, in conjunction with existing theory, can be sufficient to predict the responses of sequential hermaphrodites to harvesting pressure. Furthermore, they suggest such species can potentially adapt to size-selective harvesting.     

Patterns of flowering and sex-ratio variation in the Mediterranean shrub Phillyrea angustifolia (Oleaceae): implications for the maintenance of males with hermaphrodites

The Mediterranean shrub Phillyrea angustifolia is one of the few plants that display androdioecy, a rare breeding system in which males co-occur with hermaphrodites. However, it has been difficult to account for male frequencies previously documented for this species, which have frequently been higher than 0.5. Here we present sex-ratio data from 13 sites in Spain and Portugal that throw further light on the maintenance of androdioecy in P. angustifolia . The inferred proportion of males in these populations was around 0.3, substantially lower that 0.5 and concurring with theoretical predictions for androdioecy. Differences in the proportion of hermaphrodites in flower between "stressed" and "nonstressed" sites suggest the existence of an important life-history trade-off between fruit production and the rate at which plants recover from recurrent disturbances such as fire. The reduced frequency of flowering by hermaphrodites relative to males may help to explain the maintenance of androdioecy in this long-lived, woody species.     

High male reproductive success of hermaphrodites in the androdioecious Phillyrea angustifolia

Androdioecy, the coexistence of males and hermaphrodites within a population, is a rare breeding system, often considered as unlikely to evolve because of restrictive conditions for its maintenance. Phillyrea angustifolia, a wind-pollinated shrub, is one of the handful species reported to be androdioecious. Our previous studies have shown that natural populations of this species in southern France exhibit higher male frequencies (approximately 50%) than predicted on theoretical grounds. Thus, the male functionality of hermaphrodites is still debated. To assess the functional breeding system of this species in the wild, a paternity analysis was performed with two highly polymorphic microsatellite loci on 729 seeds collected on 10 maternal shrubs in a natural population of 24 mature individuals of P. angustifolia. A large proportion of seeds were found to have been sired by pollen from outside the population. Analysis of seeds sired by individuals within the study population revealed a high male fertility of hermaphrodites resulting in a low male advantage in fertility for male plants. Intermate distances were found to have a strong impact on male reproductive success, whereas sexual morph had no effect, with males and hermaphrodites performing equivalently. This study is the first to unequivocally document the occurrence of a male function of hermaphrodites in a natural population of an androdioecious species.     

Joint Effects of Habitat Heterogeneity and Species’ Life-History Traits on Population Dynamics in Spatially Structured Landscapes

Both habitat heterogeneity and species’ life-history traits play important roles in driving population dynamics, yet there is little scientific consensus around the combined effect of these two factors on populations in complex landscapes. Using a spatially explicit agent-based model, we explored how interactions between habitat spatial structure (defined here as the scale of spatial autocorrelation in habitat quality) and species life-history strategies (defined here by species environmental tolerance and movement capacity) affect population dynamics in spatially heterogeneous landscapes. We compared the responses of four hypothetical species with different life-history traits to four landscape scenarios differing in the scale of spatial autocorrelation in habitat quality. The results showed that the population size of all hypothetical species exhibited a substantial increase as the scale of spatial autocorrelation in habitat quality increased, yet the pattern of population increase was shaped by species’ movement capacity. The increasing scale of spatial autocorrelation in habitat quality promoted the resource share of individuals, but had little effect on the mean mortality rate of individuals. Species’ movement capacity also determined the proportion of individuals in high-quality cells as well as the proportion of individuals experiencing competition in response to increased spatial autocorrelation in habitat quality. Positive correlations between the resource share of individuals and the proportion of individuals experiencing competition indicate that large-scale spatial autocorrelation in habitat quality may mask the density-dependent effect on populations through increasing the resource share of individuals, especially for species with low mobility. These findings suggest that low-mobility species may be more sensitive to habitat spatial heterogeneity in spatially structured landscapes. In addition, localized movement in combination with spatial autocorrelation may increase the population size, despite increased density effects.     

Condition Dependent Effects on Sex Allocation and Reproductive Effort in Sequential Hermaphrodites

Theory predicts the optimal timing of sex change will be the age or size at which half of an individual''s expected fitness comes through reproduction as a male and half through reproduction as a female. In this way, sex allocation across the lifetime of a sequential hermaphrodite parallels the sex allocation of an outbreeding species exhibiting a 1∶1 ratio of sons to daughters. However, the expectation of a 1∶1 sex ratio is sensitive to variation in individual condition. If individuals within a population vary in condition, high-condition individuals are predicted to make increased allocations to the sex with the higher variance in reproductive success. An oft-cited example of this effect is seen in red deer, Cervus elaphus, in which mothers of high condition are more likely to produce sons, while those in low condition are more likely to produce daughters. Here, we show that individual condition is predicted to similarly affect the pattern of sex allocation, and thus the allocation of reproductive effort, in sequential hermaphrodites. High-condition sex-changers are expected to obtain more than half of their fitness in the high-payoff second sex and, as a result, are expected to reduce the allocation of reproductive effort in the initial sex. While the sex ratio in populations of sequential hermaphrodites is always skewed towards an excess of the initial sex, condition dependence is predicted to increase this effect.     

Sequential hermaphroditism and personality in a clonal vertebrate: the mangrove killifish

Individuals are regularly documented to consistently differ in their behavioural types (BTs). For example, some individuals are bold whereas others are shy. Within the human personality literature, the big five personality dimensions are commonly documented to be sex-specific with testosterone suggested to underpin traits such as aggressiveness. In non-human animals recent research suggests sex-specific BT expression may be influenced by ecology, mating system and sexual selection. While most research on sex-specific personality has focused on dioecious species, we explore sex differences in BT expression in a sequential hermaphrodite the mangrove killifish. We replicate within 7 isogenic genotypes and investigate sex differences (hermaphrodite and secondary male) in three BTs (exploration, boldness and aggression). This approach allows us to investigate sex differences in BT expression whilst controlling for genetic variation. In this study we find that both secondary males and hermaphrodites are repeatable at the individual level yet there was no difference between the sexes in average BT scores. Furthermore, aggression scores differed between genotypes, and were repeatable at the genotype level, suggesting strong genetic control. Finally, male boldness was significantly more repeatable than hermaphrodites potentially supporting recent proposals relating to sexual selection. We document a behavioural syndrome in male fish with bolder individuals being more aggressive, this behavioural syndrome was not observed however in hermaphrodites. In contrast to a previous developmental study in this species exploration did not correlate with either aggression or boldness in either males or hermaphrodites.     

A perfect storm: the combined effects on population fluctuations of autocorrelated environmental noise, age structure, and density dependence

While it is widely appreciated that climate can affect the population dynamics of various species, a mechanistic understanding of how climate interacts with life-history traits to influence population fluctuations requires development. Here we build a general density-dependent age-structured model that accounts for differential responses in life-history traits to increasing population density. We show that as the temporal frequency of favorable environmental conditions increases, population fluctuations also increase provided that unfavorable environmental conditions still occur. As good years accumulate and the number of individuals in a population increases, successive life-history traits become vulnerable to density dependence once a return to unfavorable conditions prevails. The stronger this ratcheting of density dependence in life-history traits by autocorrelated climatic conditions, the larger the population fluctuations become. Highly fecund species, and those in which density dependence occurs in juvenile and adult vital rates at similar densities, are most sensitive to increases in the frequency of favorable conditions. Understanding the influence of global warming on temporal correlation in regional environmental conditions will be important in identifying those species liable to exhibit increased population fluctuations that could lead to their extinction.     

Males outcompete hermaphrodites for seed siring success in controlled crosses in the polygamous Fraxinus excelsior (Oleaceae)

Polygamy (including trioecy and subdioecy), the co-occurrence of males, hermaphrodites, and females in natural populations, is a rare and poorly studied breeding system expressed in Fraxinus excelsior L. (Oleaceae), a wind-pollinated tree. Here we investigate siring ability of pollen from male vs. hermaphrodite individuals to better understand this sex polymorphism. We conducted single-donor and two-donor pollination experiments and compared both fruit set and seed siring success, assessed with polymorphic microsatellite markers, of male and hermaphrodite individuals. Single pollen donor crosses allowed us to verify the male function of hermaphrodites. However, pollen from hermaphrodites was much less proficient than male pollen, with males siring 10 times as many fruits in single donor pollination treatments. This result was strengthened by the surprisingly low reproductive success of hermaphrodites in pollen competition conditions: of the 110 seedlings analyzed three were selfed and only one was sired by the hermaphrodite donor. The remaining 106 were sired by the male pollen donor. These results raise the question of the maintenance of male fertility in hermaphrodites in Fraxinus excelsior. Male function of hermaphrodites in this species now needs to be assessed under field conditions.     

ANTAGONISTIC PLEIOTROPY: AN INTERSPECIFIC DROSOPHILA COMPARISON

Wild-type flies of 12 Drosophila species and semispecies were examined to determine whether correlation patterns between early- and late-life fitness characters predicted for individuals within a population by the antagonistic-pleiotropy hypothesis are reflected in comparisons of related species and semispecies that are known to differ in lifespan. Our goal was to determine whether the hypothesis is relevant to the evolution of life-history differences beyond the population level. Two fitness traits, egg production and percentage mating success, were observed at three ages: onset of reproductive age, one week later, and one month later. Age-dependent patterns of these traits do not consistently conform to predictions of the hypothesis. Species or semispecies that show reproductive vitality early in life need not be short-lived, and long lifespan need not be accompanied by a cost in early reproductive vitality, as measured by mating success and egg production. The two fitness traits can show different age-dependent patterns in the same species or semispecies. Potential explanations for the frequent inconsistency of the data with predictions of the hypothesis are discussed. Results support the idea that the hypothesis is only relevant to the evolution of life-history differences among individuals in the same breeding population confronted by the same environmental constraints.     

Diverse population trajectories among coexisting species of subarctic forest moths

Records of 232 moth species spanning 26 years (total catch of ca. 230,000 specimens), obtained by continuous light-trapping in Kevo, northernmost subarctic Finland, were used to examine the hypothesis that life-history traits and taxonomic position contribute to both relative abundance and temporal variability of Lepidoptera. Species with detritophagous or moss-feeding larvae, species hibernating in the larval stage, and species pupating during the first half of the growing season were over-represented among 42 species classified as abundant during the entire sampling period. The coefficients of variation in annual catches of species hibernating as eggs averaged 1.7 times higher than those of species hibernating as larvae or pupae. Time-series analysis demonstrated that periodicity in fluctuations of annual catches is generally independent of life-history traits and taxonomic affinities of the species. Moreover, closely related species with similar life-history traits often show different population dynamics, undermining the phylogenetic constraints hypothesis. Species with the shortest (1 year) time lag in the action of negative feedback processes on population growth exhibit the largest magnitude of fluctuations. Our analyses revealed that only a few consistent patterns in the population dynamics of herbivorous moths can be deduced from life-history characteristics of the species. Moreover, the diversity of population behaviour in one moth assemblage challenges any conventional wisdom suggesting predictable patterns. Our results raise several questions about perceptions and paradigms in insect population dynamics and stress the need for research on detritivorous insect population dynamics, as well as the need for more assemblage-wide studies using common trapping methods to provide comparative data on related and unrelated species with different life-history traits.     

Testing for sex differences in biparental inbreeding and its consequences in a gynodioecious species

In many gynodioecious species cross-pollinated seeds from females outperform those from hermaphrodites. Using the gynodioecious alpine perennial Silene acaulis, I investigated whether this was the result of greater biparental inbreeding among hermaphrodites leading to greater biparental inbreeding depression. I also determined the influence of relatedness on progeny fitness. Experiments were performed using individuals from a site whose population structure and coefficient of inbreeding was known. In the first experiment, crosses were made on plants in the field to determine the effect of seven different crossing distances, plus selfing, on germination and early seedling survival and growth. Although selfed seeds died more often and grew slower than crossed seeds, the effect of crossing distance was negligible for all measured fitness traits, refuting the biparental inbreeding hypothesis as a mechanism to explain why seeds from hermaphrodites die more often than those from females. Nonetheless, cross-pollinated seeds from hermaphrodites did die more, indicating that another mechanism must be responsible. In the second experiment, the effect of different levels of inbreeding on germination and seedling survival was determined by growing seeds from experimental matings varying in relatedness. Inbreeding depression for a multiplicative fitness estimate was significant for all levels of inbreeding, suggesting that inbred individuals are unlikely to become established in the population and providing insight into the results of the first experiment. Alternative hypotheses are discussed to explain why seeds from hermaphrodites die more often, which together with the results of this study, suggest that the restoration of male function in hermaphrodites comes with a correlated cost to seedling survival.     

The evolution of phally polymorphism in Bulinus truncatus (Gastropoda,Planorbidae): the cost of male function analysed through life-history traits and sex allocation

In the hermaphrodite freshwater snail Bulinus truncatus, two sexual morphs, euphallic (regular hermaphrodites) and aphallic individuals without a male copulatory organ, co-occur at various ratios in natural populations. Both aphallic and euphallic individuals can reproduce by selfing, but when outcrossing aphallic individuals can only play the female role. A comparison of life-history traits and sex allocation in these two forms provides the opportunity to investigate the evolution and maintenance of sexual polymorphisms. This study was performed to test whether a reallocation of resources from the lost male function to the female function occurs in aphallic snails at the level of both sex organs (sex allocation) and life-history traits. In a first experiment we compared life-history traits over a whole life-cycle under selfing between the two sexual morphs. In a second experiment, the sex organs were weighed to test for a difference in sex allocation between the two morphs. No difference in resource allocation to female function between the two morphs was observed in either experiment. This is in contrast to patterns frequently observed in sexually polymorphic plants, and in a previous study performed on aphally in the same snail species. We discuss the genetic and physiological hypotheses that could explain these results, and their consequences for the evolution and maintenance of phally polymorphism in B. truncatus.     

Sustainability of dioecious and hermaphrodite populations on a lattice

Sexual reproduction may be divided into two main categories: hermaphroditism and dioecy (Botany)/gonochorism (Zoology). Simultaneous hermaphrodites can function in both male and female roles whereas a dioecious/gonochorist population consists of distinct male and female individuals. Mean-field calculations, which ignore spatial aspects, suggest that self-incompatible hermaphrodites should have a twofold advantage over dioecious population when reproduction is limited by mating encounters. By use of stochastic spatial simulations we demonstrate that hermaphroditism has an even greater advantage when local interactions are considered. This result provides further support for the observation that hermaphroditism is associated with sedentary species, such as plants and animals with poor mate search efficiency. We also investigate the finite size effects associated with the well-known quadratic contact process.     

Personality and the emergence of the pace-of-life syndrome concept at the population level

The pace-of-life syndrome (POLS) hypothesis specifies that closely related species or populations experiencing different ecological conditions should differ in a suite of metabolic, hormonal and immunity traits that have coevolved with the life-history particularities related to these conditions. Surprisingly, two important dimensions of the POLS concept have been neglected: (i) despite increasing evidence for numerous connections between behavioural, physiological and life-history traits, behaviours have rarely been considered in the POLS yet; (ii) the POLS could easily be applied to the study of covariation among traits between individuals within a population. In this paper, we propose that consistent behavioural differences among individuals, or personality, covary with life history and physiological differences at the within-population, interpopulation and interspecific levels. We discuss how the POLS provides a heuristic framework in which personality studies can be integrated to address how variation in personality traits is maintained within populations.     

Sex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavioral gender and the consequences for reproduction

Although species with both male and female sexual functionsare often dichotomized into simultaneous and sequential hermaphrodites,many simultaneous hermaphrodites also exhibit sequential changesin sex allocation. In a field experiment using one such species,the gobiid fish, Lythrypnus dalli, female-biased individualsreallocated to male function in relation to their relative bodysize: consistent with the sizeadvantage hypothesis, large femaleswere more likely to reallocate and large fish had the highestspawningrates. Individuals, despite internal allocation to bothsexual functions, adopted only one behavioral gender. Behavioralmales had higher reproductive rates than behavioral females,and laboratory experiments showed that females preferred tomate with large males. Behavioral males grew more rapidly anddid notdiffer from behavioral females in survivorship. In addition,individuals who adopted male behavior but did not receive eggsin their nests maintained high levels of female tissue, whereasmales that received eggs did not. Laboratory experiments showedthat, unlike most hermaphroditic animals, L. dalli canchangeallocation either from ‘female’ to ‘male’or from ‘male’ to ‘female’. Thus, L.dalli shares haracteristics of both sequential and simultaneoushermaphrodites. Simultaneous hermaphroditism maybe maintained,in this species, to facilitate rapid sex change from femaleto male and to retain flexibility o that unsuccessful malescan revert to reproduction as females.     

A phallus for free? Quantitative genetics of sexual trade‐offs in the snail Bulinus truncatus

Resource allocation is thought to play a key role in the coexistence of different sexual morphs within hermaphroditic species. Indeed, most models assume that sexual functions are subject to a balance between reproductive advantage and energetic cost. Various types of cost (e.g. organ construction, maintenance and utilization) and levels of trade-off (physiological and genetic) may be considered. We here examine physiological and genetic costs of phallus construction and maintenance in Bulinus truncatus, a snail species in which aphallic individuals (without phallus) coexist with regular hermaphrodites. We use a quantitative genetic design involving 37 inbred lines (four populations) known to produce different proportions of aphallics, to test for the existence of genetic and nongenetic correlations between aphally and a range of life-history traits over the totality of the life cycle. Our results show that aphallic and euphallic individuals of the same line do not show consistent differences in either growth, fecundity (including offspring survival), or longevity. Furthermore, none of these traits is genetically correlated across lines with the frequency of the aphallic morph. We conclude that the cost of the construction and maintenance of the phallus must be very low in this species. Future studies should investigate the cost associated with using the phallus (i.e. male outcrossing behaviour) to explain the maintenance of high frequencies of aphallic individuals in natural populations.     

Sex expression,female frequency,and reproductive output in a gynodioecious clonal herb, <Emphasis Type="Italic">Glechoma longituba</Emphasis> (Lamiaceae)

We investigated the sex morphs and frequency of females in 24 natural populations of the clonal, gynodioecious species Glechoma longituba. In addition to the presence of hermaphrodites and females, there were some individuals with intermediate sex expression that could not be categorized as either morph. The majority of populations contained a predominance of hermaphrodites, although female frequency varied from 0 to 100%. The sexual expression of individual ramets did not change over three consecutive years or when ramets were transplanted to different populations, but it did change over the course of a flowering season. Seeds from females weighed more than those from hermaphrodites. The seed set of hermaphrodites was relatively constant across populations; the seed set of females was higher than that of hermaphrodites in most populations, but lower in populations in which females occurred at a very high frequency because of pollen limitation. This led to a negative correlation being detected between the seed set of females and the frequency of females in a population. We postulated that the adjustment of sex expression within seasons could be an adaptive mechanism of reproductive assurance in this system.     

Population dynamics of species with gynogenetic sibling species

Models are formulated for the population dynamics of a monoecious or dioecious species with an all-female parthenogenetic sibling species which is also gynogenetic. Continuous, deterministic reproduction and mortality, a stationary age distribution, random mating, and limited sexual competence for all individuals are posited. It is also supposed that in the dioecious case males do not distinguish between true and gynogenetic females. Similarly, hermaphrodites do not differentiate hermaphrodites and gynogens. The model implies that extinction is highly likely in the dioecious situation, but much less so in the monoecious one. Empirical evidence is reviewed and related to the assumptions and conclusions.