Simultaneous Hermaphrodites Research Articles

Trioecy in the Marine Mussel Semimytilus algosus (Mollusca, Bivalvia): Stable Sex Ratios Across 22 Degrees of a Latitudinal Gradient

Trioecy, the co-occurrence of males, females and hermaphrodites in natural populations, is a relatively common sexual system in plants, but is rare and poorly understood in animals. Previously, the marine mussel, Semimytilus algosus, has been described as a simultaneous hermaphrodite and there are reports of unisex animals in the wild. Here, we confirm trioecy in this bivalve, the first report of trioecy in the phylum Mollusca. We examined the frequencies of females, males and hermaphrodites in seven natural populations along a latitudinal gradient of ~2500 km and carried out a phylogenetic analysis with mussel species of the family Mytilidae with known sexual systems. Hermaphrodites (~95.3%), females (~3.6%), and males (~1.1%) were found in all seven populations across the species’ range in Chile. The consistent sex ratios across all populations suggest that the sexual system is stable in space. Phylogenetic analysis (mDNA) of members of the family Mytilidae indicates that this species alone has developed trioecy from dioecious ancestors. As unisex animals were the least common in the wild, it is likely that these animals, especially males, might be in the process of being lost in this species, and that trioecy might be an intermediate step towards gynodioecy or hermaphroditism. The reproductive characteristics of S. algosus make it an excellent model species for the study of the evolution of sexual systems in animals and also possibly the processes underlying sex determination in molluscs.

Identification of Peptides and Their GPCRs in the Peppermint Shrimp Lysmata vittata, a Protandric Simultaneous Hermaphrodite Species.

Peptide hormones commonly binding with G-protein coupled receptors (GPCRs) achieve their function in reproduction. The peppermint shrimp Lysmata vittata popular in marine ornamental trade and is known to display protandric simultaneous hermaphrodite (PSH). Knowledge on reproductive biology of this commercial species is critical for resources management and aquaculture. This study employed Illumina sequencing and bioinformatics analysis to identify peptides and their candidate GPCRs from male phase (MP) and euhermaphrodite phase (EP) of L. vittata. A total of 61 peptide and 40 peptide GPCR transcripts derive from 44 peptide families and 13 peptide GPCR families were identified, respectively. Among them, insulin-like androgenic gland hormone and crustacean female sex hormone have two unique mature peptides, respectively, and their transcripts showed higher expression levels in MP than EP, which suggest that these sex differentiation hormones might be involved in sexual characters than spermatogenesis or vitellogenesis. Overall, the first study on identification of peptides and their GPCRs in the genus Lysmata extends our knowledge of peptidergic signaling in PSH species, and provides an important basis for development of aquaculture strategies.

Is the initiation of selfing linked to a hermaphrodite\u2019s female or male reproductive function?

There is an ongoing debate about whether simultaneous hermaphrodites capable of selfing should prefer selfing over outcrossing or vice versa. While many theoretical models predict a transmission advantage for alleles that favour selfing, empirical studies often reveal low selfing rates. Despite these considerations, the underlying mechanisms that determine reproductive strategies in simultaneously hermaphroditic animals are poorly understood. In our study on the facultatively selfing free-living flatworm, Macrostomum hystrix, we ask whether the initiation of selfing, as inferred from the differential spatial distribution of received sperm, is linked to an individual’s female or male reproductive function. Specifically, the initiation of selfing could (i) be linked to the male function, when an individual is unable to donate sperm to others and hence donates sperm to self, or it could (ii) be linked to the female function, when an individual fails to receive sperm from others—and hence is unable to fertilize its eggs via outcrossing—thus inducing it to self-fertilize. We experimentally created a social environment that allowed focals to outcross via sperm donation, but simultaneously prevented them from receiving sperm—by pairing them with a partner lacking the male copulatory organ—so that fertilization of the focal’s eggs was restricted to selfing. Our results suggest that such focals generally do not initiate selfing, while we readily observe selfing in isolated worms. This suggests that in isolated M. hystrix, it is the male function that is linked to the initiation of selfing, likely due to a lack of opportunities for sperm donation.Significance statementA variety of simultaneously hermaphroditic animals are capable of reproducing via both selfing and outcrossing. While the reproductive choices of such animals can be modelled by the joint action of genetic (e.g. inbreeding depression) and ecological factors (e.g. partner availability), experimental evaluation of theoretical results is often lacking. By manipulating the social environment of focal individuals, we here provide evidence that explores the respective role that the co-occurring male and female sex functions have on the initiation of selfing in a simultaneously hermaphroditic flatworm species. Specifically, our results suggest that the initiation of selfing is linked to the worm’s male function. Insights about which function is linked to the initiation of selfing may ultimately help to better understand reproductive decisions in simultaneous hermaphrodites.

Unique mating behavior, and reproductive biology of a simultaneous hermaphroditic marine flatworm (Platyhelminthes, Tricladida, Maricola)

AbstractFlatworms generally are simultaneous hermaphrodites that exhibit various kinds of mating behavior. Here we report on the mating behavior and reproductive biology of the planarian Paucumara falcata. We recognized three phases in its mating behavior: a courtship, copulation, and postcopulatory phase. During the last‐mentioned phase, the partners showed a unique and very characteristic behavior in which their bodies intertwined, forming a spiral. Histological study of partners in copula revealed that the sclerotic tip of the musculo‐parenchymatic organ pierces the body wall of the partner and then becomes lodged in its parenchyma, suggesting that this organ may act as an anchor, thus stabilizing the worms during copulation. Similar organs in other species of marine triclad may also perform a stabilizing role during copulation. During copulation in individuals of P. falcata, sperm transfer was reciprocal or only unilateral. Copulation duration ranged 13–35 min (average 20 ± 5 min), irrespective of whether the mating was successful (i.e., resulted in the production of fertile cocoons). The spiraling phase lasted on average 10 min; some worms did not show the postcopulatory spiraling phase during their mating behavior. After successful copulation, an individual worm produced 1–12 fertile cocoons over a period of 1–17 days; from a cocoon hatched either one young (in 70% of the cases), or two young worms.

Different effects of mating group size as male and as female on sex allocation in a simultaneous hermaphrodite.

Sex allocation theory predicts that the optimal sexual resource allocation of simultaneous hermaphrodites is affected by mating group size (MGS). Although the original concept assumes that the MGS does not differ between male and female functions, the MGS in the male function (MGSm; i.e., the number of sperm recipients the focal individual can deliver its sperm to plus one) and that in the female function (MGSf; the number of sperm donors plus one) do not always coincide and may differently affect the optimal sex allocation. Moreover, reproductive costs can be split into “variable” (e.g., sperm and eggs) and “fixed” (e.g., genitalia) costs, but these have been seldom distinguished in empirical studies. We examined the effects of MGSm and MGSf on the fixed and variable reproductive investments in the sessilian barnacle Balanus rostratus. The results showed that MGSm had a positive effect on sex allocation, whereas MGSf had a nearly significant negative effect. Moreover, the “fixed” cost varied with body size and both aspects of MGS. We argue that the two aspects of MGS should be distinguished for organisms with unilateral mating.

Life history traits and reproductive performance of the caridean shrimp Lysmata boggessi, a heavily traded invertebrate in the marine aquarium industry.

The most intense commercial harvest of marine aquarium species in North America occurs in the coastal waters surrounding Florida, yet very often little information exists on the life histories, population dynamics, or reproductive characteristics of these organisms. The peppermint shrimp Lysmata boggessi is one such species and is heavily targeted along the west coast of Florida. It is known primarily among aquarists for its ability to control pest anemones and in the scientific community for its unique sexual system, protandric simultaneous hermaphroditism. However, no study has addressed fishery interactions or long-term population dynamics for L. boggessi. We used monthly fisheries-dependent sampling, with a trained observer present, for a full year to assess seasonality in sex phase ratio (males to males + hermaphrodites), size at sex change, fecundity, embryo volume and reproductive output of an exploited L. boggessi population. L. boggessi exhibited distinct seasonality in size distribution, sex phase ratio, size at sex phase change and reproductive activity. The peak reproductive season was in spring, when the population was dominated by small but fecund hermaphrodites. Reproduction decreased during fall and winter and sex phase ratios favored male phase shrimp that exhibited delayed sex change. This population and individual level information is the first of its kind for L. boggessi and fills a much needed data gap for the informed management of this fishery.

The effect of mating on female reproduction across hermaphroditic freshwater snails

AbstractSexual conflicts often arise between mating partners because each sex tries to maximize its own reproductive success. One major male strategy to influence a partner's resource allocation is the transfer of accessory gland proteins. This has been shown to occur in simultaneous hermaphrodites as well as in organisms with separate sexes. Although accessory gland proteins affect the investment of resources in both male and female function, we here specifically focus on female investment. In the great pond snail, Lymnaea stagnalis, previous studies found that the accessory gland protein ovipostatin reduced female fecundity by suppressing egg laying in the partner in the short term (days). To investigate whether this reduction in egg laying is a commonly found effect of mating in freshwater snails, we compared egg output for evidence of suppression in isolated and paired snails of eight pulmonate species. Furthermore, we determined whether the suppression of egg laying caused a shift in resource allocation to the eggs. We found that in five of the eight species egg laying was suppressed, with fewer and lighter egg masses being laid when they had access to a mating partner. In mated pairs of L. stagnalis and Biomphalaria alexandrina, allocation of resources to the eggs was altered in opposite ways: individuals of L. stagnalis laid fewer but larger and heavier eggs; individuals of B. alexandrina laid smaller and lighter eggs, with no change in egg numbers. Such changes in the female function are most likely the result of combined effects of receiving accessory gland proteins, and the cost of mating in both male and female roles. Thus, effects of the maternal environment, including the receipt of accessory gland proteins, on offspring investment are not restricted to species with separate sexes.

The Evolution of Egg Trading in Simultaneous Hermaphrodites.

Egg trading-whereby simultaneous hermaphrodites exchange each other's eggs for fertilization-constitutes one of the few rigorously documented and most widely cited examples of direct reciprocity among unrelated individuals. Yet how egg trading may initially invade a population of nontrading simultaneous hermaphrodites is still unresolved. Here, we address this question with an analytical model that considers mate encounter rates and costs of egg production in a population that may include traders (who provide eggs for fertilization only if their partners also have eggs to reciprocate), providers (who provide eggs regardless of whether their partners have eggs to reciprocate), and withholders (cheaters who mate only in the male role and just use their eggs to elicit egg release from traders). Our results indicate that a combination of intermediate mate encounter rates, sufficiently high costs of egg production, and a sufficiently high probability that traders detect withholders (in which case eggs are not provided) is conducive to the evolution of egg trading. Under these conditions, traders can invade-and resist invasion from-providers and withholders alike. The prediction that egg trading evolves only under these specific conditions is consistent with the rare occurrence of this mating system among simultaneous hermaphrodites.

Distribution patterns of the protandric simultaneous hermaphrodite, the spine-shrimp Exhippolysmata oplophoroides (Holthuis, 1948), in the Cananéia-Iguape system on the southern coast of the state of São Paulo, Brazil

Distribution patterns of the protandric simultaneous hermaphrodite, the spine-shrimp Exhippolysmata oplophoroides (Holthuis, 1948), in the Cananéia-Iguape system on the southern coast of the state of São Paulo, Brazil

Seminal Fluid-Mediated Manipulation of Post-mating Behavior in a Simultaneous Hermaphrodite

Seminal fluid proteins (SFPs) are uniquely positioned to mediate post-mating sexual selection and sexual conflict [1-3]. This role may be especially important in simultaneous hermaphrodites, in which individuals will often agree to receive sperm in order to be able to donate it, shifting the arena of sexual selection to post-mating reproductive interactions [4-7]. Nevertheless, as in separate-sexed organisms, identifying individual SFPs responsible for specific post-mating effects is difficult, owing to the complexity, rapid evolution, and functional redundancy of seminal fluid [8-11]. Here, we sought to identify SFPs that influence one striking post-mating behavior of the simultaneously hermaphroditic flatworm Macrostomum lignano, the so-called "suck behavior," in which worms respond to ejaculate receipt by placing their pharynx over their female genital opening and seemingly attempt to remove sperm and/or other ejaculate components [12-14]. We hypothesized that sucking is counter to the sperm donor's interests, potentially selecting for SFPs that reduce the suck propensity of mating partners. We tested this using a combination of quantitative genetics and RNA interference (RNAi) knockdown. As predicted, we found negative genetic correlations between the expression levels of six (outof 58) seminal fluid transcripts and partner suck propensity. RNAi knockdown confirmed that two of these transcripts, designated suckless-1 and suckless-2, indeed caused mating partners to suck less often. We suggest that these proteins are male counter-adaptations to recipient suck behavior, which itself is likely a female counter-adaptation in the ongoing evolutionary conflict to (re)gain control over ejaculate fate after mating in this hermaphroditic organism.

Sex change as a survival strategy

Sequential hermaphroditism (sex change) is understood to be a strategy that maximizes lifetime reproduction in systems where one sex confers highest fitness early in life, and the other later in life. This strategy is evolutionarily stable despite costs to growth, survival, or current reproduction. Few studies have examined advantages of sex change outside of reproduction. The mangrove rivulus fish, Kryptolebias marmoratus, presents a unique system in which to study non-reproductive consequences of sex change because reproductive opportunity decreases significantly with sex change. In natural conditions, individuals develop as self-fertilizing simultaneous hermaphrodites. Some individuals change sex to male at various points after sexual maturity, even in isolation, essentially foregoing future reproductive assurance. In a large-scale experiment that examined fitness differences among individuals exposed to ecologically relevant environmental challenges, we found that individuals that change sex from hermaphrodite to male had overwhelmingly greater chances of survival compared to those that remained hermaphrodite. Furthermore, hermaphrodites derived from lineages with higher propensities to change sex experienced greater survival advantages by changing sex. Our results indicate that sex change may be a survival strategy, one with genotype-dependent consequences.

Hermaphrodites and parasitism: size-specific female reproduction drives infection by an ephemeral parasitic castrator

Sex can influence patterns of parasitism because males and females can differ in encounter with, and susceptibility to, parasites. We investigate an isopod parasite (Hemioniscus balani) that consumes ovarian fluid, blocking female function of its barnacle host, a simultaneous hermaphrodite. As a hermaphrodite, sex is fluid, and individuals may allocate energy differentially to male versus female reproduction. We predicted the relationship between barnacle size and female reproductive function influences the distribution of parasites within barnacle populations. We surveyed 12 populations spanning ~400 km of coastline of southern California and found intermediate-sized barnacles where most likely to be actively functioning as females. While it is unclear why larger individuals are less likely to be actively reproducing as females, we suggest this reduced likelihood is driven by increased investment in male reproductive effort at larger sizes. The female function-size relationship was mirrored by the relationship between size and parasitism. We suggest parasitism by Hemioniscus balani imposes a cost to female function, reinforcing the lack of investment in female function by the largest individuals. Within the subset of suitable (=female) hosts, infection probability increased with size. Hence, the distribution of female function, combined with selection for larger hosts, primarily dictated patterns of infection.

Breeding, planktonic and settlement factors shape recruitment patterns of one of the last remaining major population of Pinna nobilis within Spanish waters

The pen shell, Pinna nobilis L., is a critically endangered bivalve threatened by mass mortality events throughout the Mediterranean, but the Alfacs Bay (Ebro Delta) still hosts many healthy individuals. Herein, we study the main factors controlling recruitment patterns in this locality, including gonadal development and abundance of critical life-stages, as well as the effect of environmental factors. Growth records from empty shells suggested a single major peak of recruitment during a period of 11 years, although many juveniles were found in two very shallow sand bars possibly acting as a barrier for water circulation and as a trap for larvae. Collectors deployed outside these sand bar areas showed zero settlers, and the availability of planktonic larvae was very low. Gonadal examination evidenced breeding throughout the summer period with successive hermaphroditism, but 20% of individuals were simultaneous hermaphrodites, a condition that has been associated with environmental stress and that could lead to in-breeding depression and potentially reduced fertility. Yet, given the large size of the population and the wide breeding period observed, planktonic processes causing larval mortality such as freshwater discharges from rice locally important rice agriculture are also proposed as possible impacts accounting for patterns of low larval availability.

Sexual pattern and caudal fin as a sexually dimorphic trait in the commercially aquacultured Meiacanthus blennies (Teleostei: Blenniidae)

AbstractThe marine aquarium industry has grown significantly and so has marine ornamental fish aquaculture. The main species targeted by commercial aquaculture are clownfish, dottybacks, gobies, and blennies. However, the limited knowledge available for the reproductive biology of several fish species hinders production, especially for blennies. Therefore, this study investigated whether two mass‐produced blenniids, Meiacanthus nigrolineatus and Meiacanthus smithi, are gonochorists and display caudal fin sexual dimorphism. For this purpose, gonadal samples and morphometric data were collected from specimens of both species kept in captivity for 6 months. Histological preparations of the whole individuals or their gonads were performed and analyzed. Results show that sex ratio does not differ from 1:1 and that gonadal development was similar to other blenniids. No evidence of sexual reversion or simultaneous hermaphroditism was found in the first 8 months of development, suggesting that both species are gonochoric. Differences in the length of upper and lower rays in the caudal fin were not detected for M. smithi, but M. nigrolineatus male individuals displayed significantly longer upper and lower rays, confirming it as a dimorphic trait for this species. The identification of the sexual pattern and sexually dimorphic traits may aid in broodstock pairing for M. nigrolineatus blennies, improving its aquaculture production and perhaps reducing some of the pressure on wild stocks.

Sexual system in the tanaidacean Falsapseudes bowmani (Crustacea: Malacostraca: Peracarida)

AbstractWith more than 40,000 species, Malacostraca is the most diverse crustacean class. Most malacostracans are gonochoristic, but simultaneous hermaphrodites are also known. Tanaidacea is one of two malacostracan orders that includes simultaneously hermaphroditic species; so far, simultaneous hermaphroditism has been confirmed externally and internally in only two tanaidacean species, both in the genus Apseudes (Apseudidae). Here we show, through external and internal morphological observations of fixed specimens, that the apseudid Falsapseudes bowmani is a simultaneous hermaphrodite, making Falsapseudes the second tanaidacean genus in which simultaneous hermaphroditism has been confirmed both externally and internally. In this species, the epistome (a projection on the clypeus) was thick and elongate in large specimens but was thin and spiniform in smaller specimens; the brooding of eggs or embryos was observed only in thin‐epistome individuals, although a pair of ovaries was confirmed in both thick‐ and thin‐epistome individuals. This suggests that individuals with a thick epistome may act as males while also retaining the female reproductive organs.

Variation in sex allocation plasticity in three closely related flatworm species.

Sex allocation (SA) theory for simultaneous hermaphrodites predicts an influence of group size on SA. Since group size can vary within an individual's lifetime, this can favor the evolution of phenotypically plastic SA. In an emerging comparative context, we here report on SA plasticity in three closely related Macrostomum flatworm species, namely Macrostomum janickei, Macrostomum cliftonensis, and Macrostomum mirumnovem. For each species, we experimentally raised worms in three group sizes (isolated, pairs, and octets) and two enclosure sizes (small and large) in all factorial combinations and studied the effects of these factors on different estimates of SA. In addition, we also evaluated whether isolated worms engage in self‐fertilization. We found that all species have plastic SA, with M. cliftonensis being more plastic than the other two species, as assessed by comparing standardized effect sizes of (a) the presence/absence of mating partners and (b) the strength of sexual competition. Moreover, we found that sperm production rate—but not sperm morphology—is plastic in M. cliftonensis, and that only M. mirumnovem self‐fertilized during our observation period. Our study suggests that both SA and SA plasticity can diverge even between closely related species.

First observations of hermaphroditism in the patellid limpetPatella piperataGould, 1846

AbstractHermaphroditism is thought to be an advantageous strategy common in marine molluscs that exhibit simultaneous, sequential or alternating hermaphroditism. Several species of patellid limpets have previously been shown to be protandrous hermaphrodites. The present study aimed to confirm whether this phenomenon occurs inPatella piperata. Transitional forms of simultaneous protandrous hermaphroditism were found in intermediate size classes ofP. piperata, in Madeira (North-eastern Atlantic). Sequential hermaphroditism was confirmed after histological analysis. The overall sex-ratio was biased towards females but approached similar proportions in the larger size classes. Analysis of size at sex change showed that at a shell length of 36 mm 50% of the population probably have changed sex. The results reported confirm the occurrence of sequential hermaphroditism. These findings are of utmost importance to the understanding of the reproductive biology of this species with direct effect on management and conservation of this traditionally harvested limpet.

Sex allocation plasticity on a transcriptome scale: Socially sensitive gene expression in a simultaneous hermaphrodite.

Phenotypic plasticity can enable organisms to produce optimal phenotypes in multiple environments. A crucial life history trait that is often highly plastic is sex allocation, which in simultaneous hermaphrodites describes the relative investment into the male versus female sex functions. Theory predicts-and morphological evidence supports-that greater investment into the male function is favoured with increasing group size, due to the increasing importance of sperm competition for male reproductive success. Here, we performed a genome-wide gene expression assay to test for such sex allocation plasticity in a model simultaneous hermaphrodite, the free-living flatworm Macrostomum lignano. Based on RNA-Seq data from 16 biological replicates spanning four different group size treatments, we demonstrate that at least 10% of the >75,000 investigated transcripts in M.lignano are differentially expressed according to the social environment, rising to >30% of putative gonad-specific transcripts (spermatogenesis and oogenesis candidates) and tail-specific transcripts (seminal fluid candidates). This transcriptional response closely corresponds to the expected shift away from female and towards male reproductive investment with increasing sperm competition level. Using whole-mount in situ hybridization, we then confirm that many plastic transcripts exhibit the expected organ-specific expression, and RNA interference of selected testis- and ovary-specific candidates establishes that these indeed function in gametogenesis pathways. We conclude that a large proportion of sex-specific transcripts in M.lignano are differentially expressed according to the prevailing ecological conditions and that these are functionally relevant to key reproductive phenotypes. Our study thus begins to bridge organismal and molecular perspectives on sex allocation plasticity.

Ontogenetic development of gonads and external sexual characters of the protandric simultaneous hermaphrodite peppermint shrimp, Lysmata vittata (Caridea: Hippolytidae).

The peppermint shrimp Lysmata vittata (Caridea: Hippolytidae) is a marine caridean shrimp popular in marine aquarium trade. The species is known to display the sexual system of protandric simultaneous hermaphrodite. In this study, based on captive bred specimens, the complete ontogenetic gonad development of L. vittata was studied both morphologically and histologically, from newly settled juveniles until they reached euhermaphrodite phase. It was found that in all specimens examined (carapace length: 1.8–8.5 mm), including the newly settled juveniles, possessed ovotestes, which comprised of an anterior ovarian and a posterior testicular part. Based on both morphological (e.g., size, color and shape) and histological features (e.g., oogenesis and spermatogenesis), four gonadal development stages were defined and described for L. vittata. From Stage I to III, the testicular part of the gonad became gradually mature but the ovarian part was still immature, which is defined as the male phase. At the male phase, cincinulli (5–8 hooks) presented at the tips of the appendix interna on the first pair of pleopods while appendices masculinae (AM), in a form of a stick structure with spines, presented at the inner edge of the appendix interna (AI) on the second pair of pleopods. At Stage IV, both the testicular part and the ovarian part were mature and hence is defined as euhermaphrodite phase. At the euhermaphrodite phase, most individuals lacked cincinulli and appendices masculinae on the first and second pair of pleopods respectively. This is the first time that complete ontogenetic gonadal and external sexual character development have been described and staged for a species from the genus Lysmata from newly settled juveniles to euhermaphrodite phase.

Sexually Antagonistic Variation and the Evolution of Dimorphic Sexual Systems.

Multicellular Eukaryotes use a broad spectrum of sexual reproduction strategies, ranging from simultaneous hermaphroditism to complete dioecy (separate sexes). The evolutionary pathway from hermaphroditism to dioecy involves the spread of sterility alleles that eliminate female or male reproductive functions, producing unisexual individuals. Classical theory predicts that evolutionary transitions to dioecy are feasible when female and male sex functions genetically trade off with one another (allocation to sex functions is sexually antagonistic) and rates of self-fertilization and inbreeding depression are high within the ancestral hermaphrodite population. We show that genetic linkage between sterility alleles and loci under sexually antagonistic selection significantly alters these classical predictions. We identify three specific consequences of linkage for the evolution of dimorphic sexual systems. First, linkage broadens conditions for the invasion of unisexual sterility alleles, facilitating transitions to sexual systems that are intermediate between hermaphroditism and dioecy (androdioecy and gynodioecy). Second, linkage elevates the equilibrium frequencies of unisexual individuals within androdioecious and gynodioecious populations, which promotes subsequent transitions to full dioecy. Third, linkage dampens the role of inbreeding during transitions to androdioecy and gynodioecy, making these transitions feasible in outbred populations. We discuss implications of these results for the evolution of dimorphic reproductive systems and sex chromosomes.