Hermaphroditism in fishes: an annotated list of species,phylogeny, and mating system

Fewer than 1% of vertebrate species are hermaphroditic, and essentially all of these are fishes. Four types of hermaphroditism are known in fishes: simultaneous (or synchronous) hermaphroditism (SH), protandry (male-to-female sex change; PA), protogyny (female-to-male sex change; PG), and bidirectional sex change (BS or reversed sex change in protogynous species). Here we present an annotated list of hermaphroditic fish species from a comprehensive review and careful re-examination of all primary literature. We confirmed functional hermaphroditism in more than 450 species in 41 families of 17 teleost orders. PG is the most abundant type (305 species of 20 families), and the others are much less abundant, BS in 66 species of seven families, SH in 55 species of 13 families, and PA in 54 species of 14 families. The recently proposed phylogenetic tree indicated that SH and PA have evolved several times in not-closely related lineages of Teleostei but that PG (and BS) has evolved only in four lineages of Percomorpha. Examination of the relation between hermaphroditism type and mating system in each species mostly supported the size-advantage model that predicts the evolution of sequential hermaphroditism. Finally, intraspecific variations in sexual pattern are discussed in relation to population density, which may cause variation in mating system.

     

Modern Portfolio Theory and the prudent hermaphrodite

Summary

Employment of Markowitz's Modern Portfolio Theory, economic models designed to predict the effect of variance and covariance on optimal investment allocation, may explain a wide variety of anomalies in reproductive biology. Natural selection appears to favor genetic diversity among offspring to a greater extent than is predicted by current theory. Consideration of the possible increase in fitness by reducing the covariance among offspring may help explain a variety of phenomena from multiple mating to the evolution of recombination (i.e., overcoming “the cost of meiosis”). Modern Portfolio Theory also make novel predictions as to when hermaphrodites should prefer the male vs. female role, i.e., engage in egg- vs. sperm-trading. It predicts that the sexual role with the lower variance in reproductive success will be preferred in hermaphrodites. This contradicts Bateman's principle that the male role is usually preferred due to energetic considerations but is consistent with Gillespie's principle. The available data suggest that mating hermaphrodites are risk-averse; gamete-trading whether of eggs or sperm is a strategy to reduce risk. In addition to overall variance, the skew of the distribution can be used to predict the mating systems of hermaphrodites and thus clarify the factors that are responsible for observed patterns of sex allocation and sexual conflict. The reduction of covariance among offspring may also help resolve “Williams' paradox”; that the observed distribution of dieoecy vs. simultaneous hermaphroditism in the Animal Kingdom cannot be explained by the prevailing models of the evolution of hermaphroditism.     

Maintenance of androdioecy in the freshwater shrimp, Eulimnadia texana: do hermaphrodites need males for complete fertilization?

Androdioecy (populations comprised of mixtures of males and hermaphrodites) is a rare mating system, found only in a few plants and animals. The rarity of this system stems from the limited benefits to males in an otherwise all-hermaphroditic population. One of the potential benefits to males is typified by the nematode Caenorhabditis elegans, in which hermaphrodites do not produce sufficient sperm to fertilize all of their eggs. Here we explore the possibility that males are needed for complete fertilization of hermaphrodites' eggs in a second androdioecious animal, the clam shrimp Eulimnadia texana. We compare the fertilization rate of outcrossed to selfed eggs to test whether the latter exhibit lower fertilization due to sperm limitation (as in C. elegans). Because this comparison confounds differences in egg fertilization due to sperm limitation with the potential for early inbreeding depression, we also used a third mating treatment, a brother/sister cross, to allow separation of sperm limitation from inbreeding depression. In both populations examined, the proportion of eggs that were fertilized decreased linearly with increasing relatedness: comparing eggs produced by outcrossing, brother/sister, and selfed matings, respectively. This pattern suggests that differences in fertilization among these three treatments were caused solely by inbreeding depression, and therefore that hermaphrodites are not sperm limited. These results are combined with previous data on this species to test whether the maintenance of males can be explained using a population genetics model specifically designed for this species.     

Sex change of primary males in a diandric labrid Halichoeres trimaculatus: coexistence of protandry and protogyny within a species

In the threespot wrasse Halichoeres trimaculatus , sex change of primary males was observed in the field and confirmed by aquarium experiments. In other words, protandry and protogyny coexisted within this species. Moreover, male-to-female-to-male sex change and female-to-male-to-female sex change were observed in aquarium experiments; i.e . reversed sex change occurred in both protandrous and protogynous hermaphrodites. These results suggest that only the direction of sex differentiation before maturation may differ between the two sexual types that have been regarded as a primary male and a protogynous hermaphrodite.     

Androdioecy and hermaphroditism in five species of clam shrimps (Crustacea: Branchiopoda: Spinicaudata) from India and Thailand

Crustaceans in the order Spinicaudata display a broad range of reproductive strategies, ranging from pure hermaphroditism to pure dioecy (separate males and females), and intermediate combinations. One particularly interesting genus of these “clam shrimps” is Eulimnadia. Based on offspring sex ratios, it has been suggested that all members of the genus are androdioecious: populations consist of mixtures of males and hermaphrodites. However, only two of the ~40 species in this genus have been examined histologically to confirm the presence of ovotestes in the purported hermaphrodites of this group. Here, we report both sex ratio and histological evidence showing that populations of five additional Eulimnadia species from India and Thailand are indeed mixes of males and hermaphrodites (four species) or hermaphrodite only (one species). Sex ratios of adults and offspring from isolated hermaphrodites are in accordance with those previously reported for 15 Eulimnadia species, and histological assays of four of the five species show the presence of both testicular and ovarian tissue in these hermaphrodites. As has been previously reported, the testicular tissue in members of these Eulimnadia spp. is located in a small section at the distal end of the gonad. In addition, the sperm produced in these hermaphrodites forms distinct plaques of compacted chromatin. Overall, these data are consistent with a single origin of hermaphroditism in Eulimnadia, and support the notion that all members of the genus are either androdioecious or all‐hermaphroditic.     

Mating frequency and resource allocation to male and female function in the simultaneous hermaphrodite land snail Arianta arbustorum

Sex allocation theory predicts that mating frequency and long‐term sperm storage affect the relative allocation to male and female function in simultaneous hermaphrodites. We examined the effect of mating frequency on male and female reproductive output (number of sperm delivered and eggs deposited) and on the resources allocated to the male and female function (dry mass, nitrogen and carbon contents of spermatophores and eggs) in individuals of the simultaneous hermaphrodite land snail Arianta arbustorum. Similar numbers of sperm were delivered in successive copulations. Consequently, the total number of sperm transferred increased with increasing number of copulations. In contrast, the total number of eggs produced was not influenced by the number of copulations. Energy allocation to gamete production expressed as dry mass, nitrogen or carbon content was highly female‐biased (>95% in all estimates). With increasing number of copulations the relative nitrogen allocation to the male function increased from 1.7% (one copulation) to 4.7% (three copulations), but the overall reproductive allocation remained highly female‐biased. At the individual level, we did not find any trade‐off between male and female reproductive function. In contrast, there was a significant positive correlation between the resources allocated to the male and female function. Snails that delivered many sperm also produced a large number of eggs. This finding contradicts current theory of sex allocation in simultaneous hermaphrodites.     

Direct reciprocity stabilizes simultaneous hermaphroditism at high mating rates: A model of sex allocation with egg trading

Simultaneous hermaphroditism is predicted to be unstable at high mating rates given an associated increase in sperm competition. The existence of reciprocal egg trading, which requires both hermaphroditism and high mating rates to evolve, is consequently hard to explain. We show using mathematical models that the presence of a trading economy creates an additional fitness benefit to egg production, which selects for traders to bias their sex allocation toward the female function. This female‐biased sex allocation prevents pure females from invading a trading population, thereby allowing simultaneous hermaphroditism to persist stably at much higher levels of sperm competition than would otherwise be expected. More generally, our model highlights that simultaneous hermaphroditism can persist stably when mating opportunities are abundant, as long as sperm competition remains low. It also predicts that reciprocity will select for heavier investment in the traded resource.     

Testing three models on the adaptive significance of protandric simultaneous hermaphroditism in a marine shrimp

Protandric simultaneous hermaphroditism, as reported for shrimps in the genus Lysmata, is a sexual system in which individuals invariably reproduce as males first and later in life as simultaneous hermaphrodites. I tested three models (i.e., sex-dependent energetic costs, sex-dependent mortality rates and sex-dependent time commitments) in an attempt to explain the adaptive value of protandric simultaneous hermaphroditism in the shrimp L. wurdemanni. Specific assumptions and predictions of each model were evaluated using manipulative experiments. In the laboratory, males grew faster than simultaneous hermaphrodites of the same size and age, an indication that the female function incurs higher energetic costs of reproduction than the male function. Also, large SHPs were more successful in monopolizing food than small males. The sex-dependent growth rate and size-dependent resource holding power agree with predictions of the sex-dependent energetic cost model. The time that simultaneous hermaphrodites required for replenishing their sperm reservoirs after mating as males was much shorter (2 days) than the time required to brood one clutch of embryos (11 days). Also, small simultaneous hermaphrodites experienced heavier mortality due to predatory fishes than large ones. The sex-dependent reproductive time commitment and size-dependent mortality agree with predictions of the sex-dependent time commitment model. Conversely, I found no evidence that the sex-dependent mortality model explains protandric simultaneous hermaphroditism in the studied species. In contrast to model predictions, mortality due to predatory fishes suffered by simultaneous hermaphrodites was not greater than that suffered by males of the same body size. In L. wurdemanni, the relationship between sex-specific investment and reproductive success seems to change during ontogeny in a way that is consistent with an adaptive adjustment of sex allocation to improve age-specific reproductive success.     

Sex allocation in a simultaneously hermaphroditic marine shrimp

Two fundamental questions dealing with simultaneous hermaphrodites are how resources are optimally allocated to the male and female function and what conditions determine shifts in optimal sex allocation with age or size. In this study, I explored multiple factors that theoretically affect fitness gain curves (that depict the relationship between sex-specific investment and fitness gains) to predict and test the overall and size-dependent sex allocation in a simultaneously hermaphroditic brooding shrimp with an early male phase. In Lysmata wurdemanni, sperm competition is absent as hermaphrodites reproducing in the female role invariably mated only once with a single other shrimp. Shrimps acting as females preferred small over large shrimps as male mating partners, male mating ability was greater for small compared to large hermaphrodites, and adolescent males were predominant in the population during the breeding season. In addition, brooding constraints were not severe and varied linearly with body size whereas the ability to acquire resources increased markedly with body size. Using sex allocation theory as a framework, the findings above permitted to infer the shape of the male and female fitness gain curves for the hermaphrodites. The absence of sperm competition and the almost unconstrained brooding capacity imply that both curves saturate, however the male curve levels off much more quickly than the female curve with increasing level of investment. In turn, the predominance of adolescent males in the population implies that the absolute gain of the female curve is greater than that of the male curve. Last, the size-dependent female preference and male mating ability of hermaphrodites determines that the absolute gain of the male curve is greater for small than for large hermaphrodites. Taking into consideration the inferred shape of the fitness gain curves, two predictions with respect to the optimal sex allocation were formulated. First, overall sex allocation should be female biased; it permits hermaphrodites to profit from the female function that provides a greater fitness return than the male function. Second, sex allocation should be size-dependent with smaller hermaphrodites allocating more than proportionally resources to male reproduction than larger ones. This size-dependent sex allocation permits hermaphrodites to profit from male mating opportunities that are the greatest at small body sizes. Size-dependent sex allocation is also expected because the male fitness gain curve decelerates more quickly than the female gain curve and experiments indicated that resources are greater for large than small hermaphrodites. These two predictions were tested when determining the sex allocation of hermaphrodites by dissecting their gonad and quantifying ovaries versus testes mass. Supporting the predictions above, hermaphrodites allocated, on average, 118 times more to the female than to the male gonad and the proportion of resources devoted to male function was higher in small than in large hermaphrodites. A trade-off between male and female allocation is assumed by theory but no negative correlation between male and female reproductive investment was observed. In L. wurdemanni, the relationship between sex-specific investment and fitness changes during ontogeny in a way that is consistent with an adjustment of sex allocation to improve size-specific reproductive success.     

Protogynous sex change in the haremic triggerfish Sufflamen chrysopterus (Tetraodontiformes)

The size-advantage model predicts that protogyny is likely to evolve in polygynous species. Polygynous mating systems have been reported from several species of triggerfishes (Balistidae), but sex change has never been confirmed among them. We performed male-removal experiments in the haremic triggerfish Sufflamen chrysopterus on the coral reefs of Sesoko Island, Okinawa. After removal and movement of territorial males, some females became single and later changed body color and sex. This is the first report of sequential hermaphroditism from Tetraodontiformes.     

The effect of cryptic female choice on sex allocation in simultaneous hermaphrodites

Sex allocation theory for simultaneous hermaphrodites has focused primarily on the effects of sperm competition, but the role of mate choice has so far been neglected. We present a model to study the coevolution of cryptic female choice and sex allocation in simultaneous hermaphrodites. We show that the mechanism of cryptic female choice has a strong effect on the evolutionary outcome: if individuals remove a fixed proportion of less-preferred sperm, the optimal sex allocation is more female biased (i.e. more biased towards egg production) than without cryptic female choice; conversely, if a fixed amount of sperm is removed, sex allocation is less female-biased than without cryptic female choice, and can easily become male biased (i.e. biased towards sperm production). Under male-biased sex allocation, hermaphroditism can become unstable and the population can split into pure males and hermaphrodites with a female-biased allocation. We discuss the idea that the evolution of sex allocation may depend on the outcome of sexual conflict over the fate of received sperm: the sperm donor may attempt to manipulate or by-pass cryptic female choice and the sperm recipient is expected to resist such manipulation. We conclude that cryptic female choice can have a strong influence on sex allocation in simultaneous hermaphrodites and strongly encourage empirical work on this question.     

Sexual selection: lessons from hermaphrodite mating systems

Over the last 130 years, research has established that (a) sexualselection exists and is widespread in the plant and animal kingdoms;(b) it does not necessarily entail sexual dimorphism; even hermaphroditeshave it; (c) it does not require intelligence or a sophisticatedsense of esthetics; even tapeworms and plants choose mates;and (d) it does not require brawn or even mobility for competition;plants may compete for pollinators, and broadcast spawning invertebratesmay also compete for matings. Although discussions of sexualselection often focus on sexual dimorphism, several phenomenathat are commonly associated with sexual selection are widespreadand highly developed in hermaphrodites. These phenomena include(a) bizarre and expensive courtship and copulatory behavior,(b) multiple mating and sperm competition, (c) rapid evolutionof genitalia, (d) special structures associated with courtship,and (e) sexual polymorphism. The skewed breeding sex ratiosassociated with sequential hermaphroditism have long been recognizedas contributory to sexual selection. In many simultaneous hermaphrodites,although the sex ratio at mating may be one to one, the actualreproductive sex ratio may also be skewed, creating a high potentialfor sexual selection. Reproductive biology in hermaphroditictaxa also involves a lot of complexity unknown in dioecioustaxa, such as sex change, facultative sex allocation and conditionalreciprocity that offers opportunities to enrich our understandingof sexual selection and to test the assumptions and predictionsof theory.     

The ovotestis: an underdeveloped organ of evolution

In animals that have separate sexes (gonochorists), many sperm are produced to fertilise a few eggs. As the male germline undergoes more mitoses, so the accumulated mutation frequency is elevated in sperm compared with ova, and evolution is 'male-driven'. In contrast, in many hermaphroditic animals, a single organ--the ovotestis--produces both ova and sperm. Since self-renewing cells in the ovotestis may give rise to both cell types throughout life, ova in hermaphrodites could in theory have undergone as many cell divisions as sperm. Here, I consider some possible effects of the ovotestis on evolution. In particular, I hypothesise that the accumulated mutation frequency of nuclear genes in hermaphrodites (including species that change sex) may reach twice that compared with gonochorists. There may be an even greater increase in the mitochondrial mutation frequency. Further developmental studies and the accumulation of comparative data should allow hypothesis testing. If the prediction is correct, then it may provide the most-straightforward explanation for the extraordinary diversity of mitochondrial DNA in some hermaphrodites, especially molluscs.     

Intersexual conflict in androdioecious clam shrimp: Do androdioecious hermaphrodites evolve to avoid mating with males?

A recent sexual conflict model posits that a form of intersexual conflict may explain the persistence of males in androdioecious (males + hermaphrodites) populations of animals that are being selected to transition from dioecious (gonochoristic) mating to self‐compatible hermaphroditism. During the evolutionary spread of a self‐compatible hermaphrodite to replace females, the selective pressures on males to outcross are in conflict with the selective pressures on hermaphrodites to self. According to this model, the unresolved conflict interferes with the evolutionary trajectory from dioecy to hermaphroditism, slowing or halting that transition and strengthening the otherwise “transitory” breeding system of androdioecy into a potentially stable breeding strategy. Herein, we assess this model using two dioecious and two androdioecious clam shrimp (freshwater crustaceans) to ask two questions: (1) Have hermaphrodites evolved so that males cannot effectively recognize them?; and (2) Do androdioecious hermaphrodites avoid males? Androdioecious males made more mistakes than dioecious males when guarding potential mates suggesting that androdioecious males were less effective at finding hermaphrodites than dioecious males were at finding females. Similarly, in a three‐chambered experiment, focal hermaphrodites chose to aggregate with their same sex, whereas focal dioecious males chose to aggregate with the alternate sex. Together, these two experiments support the sexual conflict model of the maintenance of androdioecy and suggest that hermaphrodites are indeed evolving to avoid and evade males.     

The timing of spawning and egg production as constraints on male mating success in a simultaneously hermaphroditic fish

Synopsis The evolutionary stability of simultaneous hermaphroditism depends in part on the existence of constraints on the potential for male mating success. In the seabasses (Serranidae), several species of simultaneous hermaphrodites divide each day's clutch of eggs into parcels that are spawned sequentially and alternately with a partner. This behavior is thought to be one source of constraint on male mating success. A possible related source is the pattern of egg production. A study was therefore performed on the chalk bass,Serranus tortugarum, to examine this pattern. The results indicate that eggs are readied for spawning gradually over the course of the daily spawning period. The pattern of egg production acts jointly with spawning behavior in constraining male mating success. This pattern may be a pre-existing state to which the mating system has been adjusted, or it may have co-evolved with the mating system.     

Why do female migratory birds arrive later than males?

1. In migratory birds males tend to arrive first on breeding grounds, except in sex-role reversed species. The two most common explanations are the rank advantage hypothesis, in which male-male competition for breeding sites drives stronger selection for early arrival in males than females, and the mate opportunity hypothesis, which relies on sexual selection, as early arrival improves prospects of mate acquisition more for males than for females. 2. To date, theoretical work has focused on selection for early arrival within a single sex, usually male. However, if fitness depends on territory quality, selection for early arrival should operate on both sexes. Here we use two independent modelling approaches to explore the evolution of protandry (male-first arrival) and protogyny (female-first arrival) under the rank advantage and mate opportunity hypotheses. 3. The rank advantage hypothesis, when operating alone, fails to produce consistent patterns of protandry, despite our assumption that males must occupy territories before females. This is because an individual of either sex benefits if it out-competes same-sex competitors. Rather than promoting protandry, the rank advantage mechanism can sometimes result in protogyny. Female-female competition is stronger than male-male competition early in the season, if females compete for a resource (territories occupied by males) that is initially less common than the resource of interest to males (unoccupied territories). 4. Our results support the mate opportunity hypothesis as an explanation of why protandry is the norm in migratory systems. Male-biased adult sex ratios and high levels of sperm competition (modelled as extra-pair young: EPY) both produce protandry as a result of sexual selection. Protogyny is only observed in our models with female-biased sex ratios and low EPY production. 5. We also show that the effects of sex ratio biases are much stronger than those of EPY production, explore the evidence for sex ratio biases and extra-pair paternity in migratory species and suggest future research directions.     

Mating group size and evolutionarily stable pattern of sexuality in barnacles

Barnacles, marine crustaceans, have various patterns of sexuality depending on species including simultaneous hermaphroditism, androdioecy (hermaphrodites and dwarf males), and dioecy (females and dwarf males). We develop a model that predicts the pattern of sexuality in barnacles by two key environmental factors: (i) food availability and (ii) the fraction of larvae that settle on the sea floor. Populations in the model consist of small individuals and large ones. We calculate the optimal resource allocation toward male function, female function and growth for small and large barnacles that maximizes each barnacle's lifetime reproductive success using dynamic programming. The pattern of sexuality is defined by the combination of the optimal resource allocations. In our model, the mating group size is a dependent variable and we found that sexuality pattern changes with the food availability through the mating group size: simultaneous hermaphroditism appears in food-rich environments, where the mating group size is large, protandric simultaneous hermaphroditism appears in intermediate food environments, where the mating group size also takes intermediate value, the other sexuality patterns, androdioecy, dioecy, and sex change are observed in food-poor environments, where the mating group size is small. Our model is the first one where small males can control their growth to large individuals, and hence has ability to explain a rich spectrum of sexual patterns found in barnacles.     

Optimal sex allocation under pollen limitation

Most flowering plants are simultaneous hermaphrodites. Within species and even within local populations, sex allocation is usually highly plastic. Here, we link pollen sufficiency to the size of pollen-exchanging groups (i.e., pollen neighborhoods) and to pollen transfer efficiency, using an individual-based game-theoretic framework to determine the stable distribution of sex allocation that does not require the unrealistic assumption of infinitely large, panmictic populations. In the absence of selfing, we obtain the novel result that pollen limitation destabilizes hermaphroditism and favors separate sexes, whereas hermaphroditism remains stable without pollen limitation. With mixed mating, hermaphroditism is stable except when the fitness value of selfed offspring is less than half that of outcrossed offspring (i.e., strong inbreeding depression). In that case, the size of pollen neighborhoods, pollen transfer efficiencies, and the relative fitness of selfed offspring determine whether separate sexes or hermaphroditism is the stable outcome. The model thus predicts that separate sexes can derive from either of two ancestral states: obligate outcrossing under pollen limitation, or mixed mating (competing self-fertilization) under severe inbreeding depression. It also predicts conditions under which variance in sex-allocation among hermaphrodites within pollen exchanging groups along a gradient of pollen limitation can range from high (dioecy) to near zero (equal proportions of male and female investment).     

Barriers to outcrossing success in the primarily self-fertilizing clam shrimp, Eulimnadia texana (Crustacea, Branchiopoda)

Abstract. The expected proportion of males in androdioecious populations (those comprised of males and hermaphrodites) largely depends on the fertilization opportunities of males. If male mating opportunities are low due to restricted access to hermaphroditic eggs, then populations will be hermaphrodite-biased. Hermaphrodites have two mechanisms available to limit male mating success: (1) pre-mating barriers to outcrossing, in which hermaphrodites choose not to pair with males and (2) post-mating barriers to outcrossing, in which hermaphrodite sperm has greater access to eggs than male sperm. In this study, we measured male mating success in the androdioecious clam shrimp Eulimnadia texana when pre-mating barriers to outcrossing were removed. These branchiopod crustaceans are small (5–8 mm), filter feeders that live in ephemeral pools in the deserts of the southwestern United States. Using genetic markers, we measured male mating success in laboratory experiments in two populations of these shrimp. We correlated mating success with clasping time, clasping during egg transfer, and male thrusting during egg transfer. Males fertilized an average of 24–40% of the hermaphrodites' eggs. Outcrossing success was positively correlated with clasping duration, and was nearly an order of magnitude higher for males thrusting during egg transfer relative to thrusting at other times during pairing. Because these estimates of mating success were similar to previously reported estimates (in which both pre- and post-mating barriers to outcrossing were potentially important), we deduced that pre-mating barriers to outcrossing do not greatly decrease male outcrossing success in E. texana ; the low fertilization (25–50% of available eggs) by males is thus due to post-mating barrier(s) to outcrossing.     

Sexual systems and life history of barnacles: a theoretical perspective

Thoracican barnacles show one of the most diverse sexual systems in animals: hermaphroditism, dioecy (males and females), and androdioecy (males and hermaphrodites). In addition, when present, male barnacles are very small and are called "dwarf males". The diverse sexual systems and male dwarfism in this taxon have attracted both theoretical and empirical biologists. In this article, we review the theoretical studies on barnacles' sexual systems in the context of sex allocation and life history theories. We first introduce the sex allocation models by Charnov, especially in relation to the mating group size, and a new expansion of his models is also proposed. We then explain three studies by Yamaguchi et al., who have studied the interaction between sex allocation and life history in barnacles. These studies consistently showed that limited mating opportunity favors androdioecy and dioecy over hermaphroditism. In addition, other factors, such as rates of survival and availability of food, are also important. We discuss the importance of empirical studies testing these predictions and how empirical studies interact with theoretical constructs.