Hermaphroditic fishes are almost exclusively sequential—simultaneous hermaphroditism is only known to occur in a few fishes, such as the
Rivulid killifish
Kryptolebias marmoratus and
hamlets.
Teleost fishes are the only vertebrate
lineage where sequential hermaphroditism occurs. However, protandry features a spectrum of different forms, which are characterized by the overlap between male and female reproductive function throughout an organism's lifetime: • Protandrous sequential hermaphroditism: Early reproduction as a pure male and later reproduction as a pure female. • Protandrous hermaphroditism with overlap: Early reproduction as a pure male and later reproduction as a pure female with an intervening overlap between both male and female reproduction. • Protandrous simultaneous hermaphroditism: Early pure male reproduction and later reproduction in both sexes. Furthermore, there are also species that reproduce as both sexes throughout their lifespans (i.e
simultaneous hermaphrodites), but shift their reproductive resources from male to female over time.
Protandrous examples Protandry occurs in a widespread range of animal phyla. In fact, protandrous hermaphroditism occurs in many fish,
mollusks, but is completely absent in terrestrial vertebrates. If the female dies, in many cases, the reproductive male gains weight and becomes the female for that group. The largest non-breeding male then sexually matures and becomes the reproductive male for the group. The
ribbon eel also goes through a protandrous life cycle. and in the orders
Clupeiformes,
Siluriformes, and
Stomiiformes. Since these groups are distantly related and have many intermediate relatives that are not protandrous, it strongly suggests that protandry evolved multiple times. Phylogenies support this assumption because ancestral states differ for each family. For example, the ancestral state of the family Pomacentridae was gonochoristic (single-sexed), indicating that protandry evolved within the family. • The flatworms
Hymanella retenuova. •
Laevapex fuscus, a
gastropod, is described as being functionally protandric. The
sperm matures in late winter and early spring, the eggs mature in early summer, and
copulation occurs only in June. This shows that males cannot reproduce until the females appear, thus why they are considered to be functionally protandric. •
Speyeria mormonia, the Mormon fritillary, is a butterfly species exhibiting protandry. In its case, functional protandry refers to the emergence of male adults 2–3 weeks before female adults. • Members of the shrimp genus
Lysmata perform protandric simultaneous hermaphroditism where they become true hermaphrodites instead of females.'', a genus of shrimp that performs protandric simultaneous hermaphroditism
Protogyny ,
Thalassoma lunare, a protogynous animal species Protogynous hermaphrodites are animals that are born female and at some point in their lifespan change sex to male. Protogyny is a more common form of sequential hermaphroditism in fish, especially when compared to protandry. As the animal ages, it shifts sex to become a male animal due to internal or external triggers, undergoing physiological and behavioral changes. In many fishes, female
fecundity increases continuously with age, while in other species larger males have a selective advantage (such as in harems), so it is hypothesized that the mating system can determine whether it is more selectively advantageous to be a male or female when an organism's body is larger. About 75% of the 500 known sequentially hermaphroditic fish species are protogynous and often have polygynous mating systems. In these systems, large males use aggressive territorial defense to dominate female mating. This causes small males to have a severe reproductive disadvantage, which promotes strong selection of size-based protogyny. Therefore, if an individual is small, it is more reproductively advantageous to be female because they will still be able to reproduce, unlike small males. Common model organisms for this type of sequential hermaphroditism are
wrasses. They are one of the largest families of coral reef fish and belong to the family Labridae. Wrasses are found around the world in all marine habitats and tend to bury themselves in sand at night or when they feel threatened. In wrasses, the larger of a mating pair is the male, while the smaller is the female. In most cases, females and immature males have a uniform color while the male has the terminal bicolored phase. In other words, both the initial- and terminal-phase males can breed, but they differ in the way they do it. In the
California sheephead (
Semicossyphus pulcher), a type of wrasse, when the female changes to male, the ovaries degenerate and spermatogenic crypts appear in the gonads. The general structure of the gonads remains ovarian after the transformation and the sperm is transported through a series of ducts on the periphery of the gonad and
oviduct. Here, sex change is age-dependent. For example, the California sheephead stays a female for four to six years before changing sex since all California sheephead are born female.
Bluehead wrasses begin life as males or females, but females can change sex and function as males. Young females and males start with a dull initial-phase coloration before progressing into a brilliant terminal-phase coloration, which has a change in intensity of color, stripes, and bars. Terminal-phase coloration occurs when males become large enough to defend territory. Initial-phase males have larger
testes than larger, terminal phase males, which enables the initial-phase males to produce a large amount of sperm. This strategy allows these males to compete with the larger territorial male.
Botryllus schlosseri, a colonial
tunicate, is a protogynous hermaphrodite. In a colony, eggs are released about two days before the peak of sperm emission. Although self-fertilization is avoided and cross-fertilization favored by this strategy, self-fertilization is still possible. Self-fertilized eggs develop with a substantially higher frequency of anomalies during cleavage than cross-fertilized eggs (23% vs. 1.6%). Other examples of protogynous organisms include: • In the following
fish families:
Serranidae (groupers),
Sparidae (porgies),
Synbranchidae (swamp eels),
Labridae (wrasses),
Pomacanthidae (angelfishes),
Gobiidae (gobies),
Lethrinidae (emperors), and possibly others. • The intertidal
isopod Gnorimosphaeroma oregonense. • Protogyny sometimes occurs in the frog
Rana temporaria, where older females will sometimes switch to being males.
Size-advantage model The size-advantage model states that individuals of a given sex reproduce more effectively if they are a certain size or age. To create selection for sequential hermaphroditism, small individuals must have higher reproductive fitness as one sex and larger individuals must have higher reproductive fitness as the opposite sex. For example, eggs are larger than sperm, thus larger individuals are able to make more eggs, so individuals could maximize their reproductive potential by beginning life as male and then turning female upon achieving a certain size. Warner suggests that selection for protandry may occur in populations where female fecundity is augmented with age and individuals mate randomly. Selection for protogyny may occur where there are traits in the population that depress male fecundity at early ages (territoriality, mate selection or inexperience) and when female fecundity is decreased with age, the latter seems to be rare in the field. In 2009, Kazanciglu and Alonzo found that dioecy was only favored when the cost of changing sex was very large. This indicates that the cost of sex change does not explain the rarity of sequential hermaphroditism by itself. The size-advantage model also explains under which mating systems protogyny or protandry would be more adaptive. In a haremic mating system, with one large male controlling access to numerous females for mating, this large male achieves greater reproductive success than a small female as he can fertilize numerous batches of eggs. So in this kind of haremic mating system (such as many wrasses), protogyny is the most adaptive strategy ("breed as a female when small, and then change to male when you're large and able to control a harem"). In a paired mating system (one male mates with one female, such as in clownfish or moray eels) the male can only fertilize one batch of eggs, whereas the female needs only a small male to fertilize her batch of eggs. so the larger she is, the more eggs she'll be able to produce and have fertilized. Therefore, in this kind of paired mating system, protandry is the most adaptive strategy ("breed as a male when small, and then change to female when you're larger").
Protection against inbreeding Sequential hermaphroditism can also protect against inbreeding in populations of organisms that have low enough motility and/or are sparsely distributed enough that there is a considerable risk of siblings encountering each other after reaching sexual maturity, and interbreeding. If siblings are all the same or similar ages, and if they all begin life as one sex and then transition to the other sex at about the same age, then siblings are highly likely to be the same sex at any given time. This should dramatically reduce the likelihood of inbreeding. Both protandry and protogyny are known to help prevent inbreeding in plants, Many studies also involve understanding the effect of aromatase inhibitors on sex change. One such study was performed by Kobayashi et al. In their study they tested the role of estrogens in male three-spot wrasses (
Halichoeres trimaculatus). They discovered that fish treated with aromatase inhibitors showed decreased gonadal weight, plasma estrogen level and spermatogonial proliferation in the testis as well as increased androgen levels. Their results suggest that estrogens are important in the regulation of
spermatogenesis in this protogynous hermaphrodite. Previous studies have also investigated sex reversal mechanisms in
teleost fish. During sex reversal, their whole gonads including the germinal epithelium undergoes significant changes, remodeling, and reformation. One study on the teleost
Synbranchus marmoratus found that
metalloproteinases (MMPs) were involved in gonadal remodeling. In this process, the ovaries degenerated and were slowly replaced by the germinal male tissue. In particular, the action of MMPs induced significant changes in the interstitial gonadal tissue, allowing for reorganization of germinal epithelial tissue. The study also found that
sex steroids help in the sex reversal process by being synthesized as
Leydig cells replicate and differentiate. Thus, the synthesis of sex steroids coincides with gonadal remodeling, which is triggered by MMPs produced by germinal epithelial tissue. These results suggests that MMPs and changes in steroid levels play a large role in sequential hermaphroditism in teleosts.
Genetic consequences Sequential hermaphrodites almost always have a sex ratio biased towards the birth sex, and consequently experience significantly more reproductive success after switching sexes. According to the population genetics theory, this should decrease
genetic diversity and
effective population size (Ne). However, a study of two ecologically similar
santer sea bream (
gonochoric) and
slinger sea bream (protogynous) in South African waters found that genetic diversities were similar in the two species, and while Ne was lower in the instant for the sex-changer, they were similar over a relatively short time horizon. The ability of these organisms to change biological sex has allowed for better reproductive success based on the ability for certain genes to pass down more easily from generation to generation. The change in sex also allows for organisms to reproduce if no individuals of the opposite sex are already present. ==Botany==