Sachi Yamaguchi

Diverse, Continuous, and Plastic Sexual Systems in Barnacles

Barnacles (Crustacea: Thoracica) show diverse sexual systems, including simultaneous hermaphroditism, androdioecy (hermaphrodites + males), and dioecy (females + males). When males occur, they are always much smaller (called dwarf males) than conspecific hermaphrodites or females. Ever since Darwin made this discovery, many scientists have been fascinated by such diversity. In this study, we provide an overview of (1) the diversity of sexual systems in barnacles, (2) the continuity between different sexual systems in some genera or species, and (3) the plasticity in sexual expression in several species. First, although most barnacles are hermaphroditic, both theoretical and empirical studies suggest that females and dwarf males tend to occur in species with small mating groups. Low sperm competition among hermaphrodites and little chance to act as a male are both associated with small group sizes and identified as the forces promoting the evolution of dwarf males and pure females, respectively. Second, in some groups of barnacles, the distinction between hermaphrodites and dwarf males is unclear because of the potential of dwarf males to become hermaphrodites. As many barnacle species tend toward protandric simultaneous hermaphroditism (develop male function first and then add female function without discarding male function), the dwarf males in such cases are best described as potential hermaphrodites that arrest growth and emphasize male function much earlier because of attachment to conspecifics. This is presumably advantageous in fertilizing the eggs of the host individuals. The distinction between hermaphrodites and females may also be obscured in some species. Third, sex allocation and penial morphology are plastic in some species. We also report the results of a transplanting experiment on small individuals of the pedunculate barnacle Octolasmis angulata, which suggests that individuals transplanted onto conspecifics developed longer and broader penises than did control individuals. Overall, the diversity, continuity, and plasticity in the sexual systems of barnacles are sources of important insights into the evolution and maintenance of the diversity of sexual systems.

Dwarf males and hermaphrodites can coexist in marine sedentary species if the opportunity to become a dwarf male is limited

In many marine sedentary species, dwarf males coexist with large individuals who are either hermaphrodites or females. Simple models of the evolutionary game of sex allocation and life history choice predict that stable coexistence of dwarf males and hermaphrodites is rather difficult. In many of these models, however, newly settled larvae are assumed to choose freely between becoming a dwarf male or an immature fast growing individual. In this paper, we consider a new model in which the opportunity for a newly settled individual to become a dwarf male is limited, for example by the scarcity of large individuals near its settlement site. In the evolutionarily stable strategy, the stationary population is either (1) dominated by hermaphrodites, with dwarf males scarce or absent, if immature individuals are fast-growing, (2) a mixture of dwarf males and large females, if larval growth is slow and the opportunity to become dwarf males is high, (3) a mixture of dwarf males and hermaphrodites, if larval growth is slow and the opportunity to become dwarf males is limited. We also examine the case in which the opportunity to be a growing individual is spatially limited.

Sperm as a paternal investment: a model of sex allocation in sperm-digesting hermaphrodites

Some simultaneously hermaphroditic animals are known to digest received sperm. To investigate the effect of sperm digestion on the sex allocation of simultaneous hermaphrodites, we constructed models about evolutionarily stable resource allocation between male and female functions. We assumed that resource obtained from sperm digestion is used for gametogenesis (sperm and/or egg production). As a result, we found that sperm digestion increases the evolutionarily stable allocation to male function under finite number of matings. This is because excess sperm function as nuptial gift or paternal investment when at least a fraction of digested sperm is translated into eggs. Therefore, some factors which affect the assurance of paternity for sperm donors, such as cryptic female choice and/or sperm displacement, may change the result. In addition, this result implies that sperm digestion does not necessarily make male role less preferred. Further studies on the usage of donated sperm are required to test the validity of our models.

Time required for sex change in teleost fishes: Hormonal dynamics shaped by selection

Bidirectional sex change is observed in many teleost fish. When social conditions change, the sex transition may take place over a period of several days to a few months. To understand temporal differences for sex change in either direction, I propose a simple mathematical model for the hormone-enzyme dynamics. Aromatase (P450arom) catalyses the synthesis of estradiol from testosterone. I assume that a change in social conditions for individuals affects the rates of production and degradation of P450arom. I then consider the evolution of parameters in the dynamics. Optimal parameter values are those that minimize total fitness cost, defined as the sum of fitness losses due to delay in being a functional male or female, and the cost of accelerated degradation of P450arom in changing from female to male sex. The model predicts that, in haremic species, sex change promotes a faster degradation of P450arom, resulting in a faster female-to-male transition than male-to-female transition. In contrast, in monogamous species, or with a small number of females, there is no benefit in a faster degradation of P450arom when changing to male, resulting in approximately equal timespans for sex change in either direction.

Evolution of sex determination and sexually dimorphic larval sizes in parasitic barnacles

The parasitic (rhizocephalan) barnacles include species of which larval sex is determined by the mother (genetic sex determination, GSD), male larvae are larger than female larvae, and a female accepts only two dwarf males who sire all the eggs laid by her. In contrast, other species of parasitic barnacles exhibit monomorphic larvae that choose to become male or female depending on the condition of the host they settle (environmental sex determination, or ESD), and a female accepts numerous dwarf males. Here, we ask why these set of traits are observed together, by examining the evolution of sex determination and the larval size. ESD has an advantage over GSD because each larva has a higher chance of encountering a suitable host. On the other hand, GSD has two advantages over ESD: the larval size can be chosen differently between sexes, and their larvae can avoid spending time for sex determination on the host. We conclude that, in species whose female accepts only two males, the male larvae engage in intense contest competition for reproductive opportunities, and males success-size relation is very different from females. Then, larvae with predetermined sex (GSD) with sexually dimorphic larvae is more advantageous than ESD. In contrast, in species whose females accept many dwarf males, the competition among males is less intense, and producing larvae with undetermined sex should evolve. We also discuss the condition for females to evolve receptacles to limit the number of males she accepts.

Advantage for the sex changer who retains the gonad of the nonfunctional sex

Many species of teleost fish live in coral reefs and change sex depending on their social status; some even demonstrate sex change in both directions. Typically, in the absence of a more dominant competitive individual, the fish functions as a male; however, when a more competitively superior individual arrives, the focal fish becomes a female. Among these bidirectional sex changers, there are species that retain the gonads of the currently nonfunctional sex, i.e., a male retains female reproductive tissues or a female retains male reproductive tissues. We construct a game-theoretic model and examine the conditions under which gonads of both the functional and the nonfunctional sex would be kept. We observe that a focal fish always retains both gonads when the social conditions change frequently in either direction, while it retains only the gonads of the currently functional sex when there is an infrequent change of social conditions. However, in order to explain the observed patterns of a monogamous goby Paragobiodon echinocephalus that undergoes a complete reconstruction of the entire gonad during sex change and a polygynous goby Trimma okinawae that retains the gonad of the nonfunctional sex, we need to assume that the cost of a male retaining the female gonad is much less than that of a female retaining a male gonad. We argue that this assumption is plausible given structural differences in male and female fitness payoffs.Significance StatementAmong coral fish that exhibit bidirectional sex change, some retain the gonad of the nonfunctional sex as well as the current sex, while others exhibit the gonad of the current sex only. A game-theoretic model was developed to investigate under what conditions we might expect a bidirectional sex changer should keep the gonad of the nonfunctional sex. The frequency of sex change opportunity, the time required to reconstruct the gonad, and the maintenance cost all affect the evolution of gonad retention. A quantitative parameterization of the model for well-studied species concluded that the cost for a male to keep a female gonad must be much smaller than the cost for a female to retain a male gonad. The results demonstrated the importance of combining physiological and morphological aspects in the evolutionary ecology of sex changing fish.

Sexual system of a symbiotic pedunculate barnacle Poecilasma kaempferi (Cirripedia: Thoracica)

Abstract The pedunculate barnacle Poecilasma kaempferi lives on the body surface of deep-sea decapod crustaceans. We observed that some individuals of this species are attached to conspecifics and investigated their reproductive status to determine whether such individuals are functional dwarf males, as reported for other pedunculates. We also experimentally evaluated the effect of attachment site (whether directly attached to the substratum, attached to conspecifics, or in contact with conspecifics) on reproductive status in an aquarium experiment. Both approaches demonstrated that in this species, conspecific-attached individuals are not dwarf males and are indistinguishable from other individuals in terms of reproductive status. Thus, this species should be considered hermaphroditic rather than androdioecious (i.e. males + hermaphrodites). Such conspecific-attached hermaphrodites may represent an example of pre-adaptation for the evolution of dwarf males.

Be a good loser: A theoretical model for subordinate decision-making on bi-directional sex change in haremic fishes

Among animals living in groups with reproductive skew associated with a dominance hierarchy, subordinates may do best by using various alternative tactics. Sequential hermaphrodites or sex changers adopt a unique solution, that is, being the sex with weaker skew when they are small and subordinate, and changing sex when they become larger. In bi-directionally sex-changing fishes, although most are haremic and basically protogynous, subordinate males can change sex to being females. We study a mathematical model to examine when and why such reversed sex change is more adaptive than dispersal to take over another harem. We attempt to examine previously proposed hypotheses that the risk of dispersal and low density favor reversed sex change, and to specify an optimal decision-making strategy for subordinates. As a result, while the size-dependent conditional strategy in which smaller males tend to change sex is predicted, even large males are predicted to change sex under low density and/or high risk of dispersal, supporting both previous hypotheses. The importance of spatiotemporal variation of social and ecological conditions is also suggested. We discuss a unified framework to understand hermaphroditic and gonochoristic societies.

Why is bidirectional sex change rare

Various species of fish living in coral reef communities show sequential hermaphroditism, or sex change. In a typical case, an individual first matures as a female, and later, when it becomes dominant in the mating group, it becomes a male (i.e., protogynous sex change). Many species show only unidirectional changes but some of coral reef fishes exhibit bidirectional sex changes, in which even a dominant male may revert to female when a socially more dominant competitor arrives. However, bidirectional sex change has rarely been observed in natural conditions, even among those species exhibiting it under experimental conditions. Here we explain the rarity of bidirectional sex change by studying dynamics of hormones controlling sex expression. We consider social status factor, SF, which is elevated when the individual becomes more dominant in the mating group. When the SF level is high, the dynamics would culminate with low estradiol expression and high testosterone expression, suggesting a male phenotype. In contrast, when SF level is low, the system converges to an equilibrium with high estradiol expression and low testosterone expression, suggesting a female phenotype. There is a parameter region in which the dynamics exhibit bistability. The model demonstrates hysteresis: as SF increases smoothly, the system undergoes a sudden transition in the levels of sex hormones. The model can explain why species show unidirectional sex change, in that an individuals switch to a new sex is irreversible, even if the individuals social situation returns to the original subdominant status.

Temperature-dependent sex determination, realized by hormonal dynamics with enzymatic reactions sensitive to ambient temperature

Temperature-dependent sex determination (TSD) is adopted by many animal taxa, including reptiles and fishes. In some species, the eggs develop into females under a low hatching temperature, whereas they will develop into males under a high hatching temperature (called the FM-pattern). In other species, the eggs develop into males (or females) under a low (or high) hatching temperature (MF-pattern). Still, in other species, the eggs develop into females, males, or females, respectively, when under a low, intermediate, or high hatching temperature (FMF-pattern). In this paper, we study a mechanism for realizing TSD. Specifically, we explore a hypothesis that the temperature dependence of enzymatic reaction rates causes a clear switching of sex hormone levels with gradual change of temperature. Herein, we analyze a simple hormonal-dynamics with temperature-sensitive rates of enzymatic reactions included in the sex-determining gene-protein regulatory network. We first examined the cases in which the enzymatic reactions followed Arrhenius equation. The MF-pattern appeared when the rates of aromatase production and/or estradiol production depend more strongly on temperature than do the rates of their decay. By contrast, the FM-pattern appeared when the temperature dependence is stronger for the decay rates of aromatase and/or estradiol than their production rates. However, the FMF-pattern appeared only when some enzymatic reactions follow Berthelot-Hood equation, which exhibits a stronger temperature dependence under higher temperatures than Arrhenius equation. We discuss the possible mechanisms for TSD of FMF-pattern, including alternative splicing and post-translational modification.