Sequential Hermaphroditism
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Sequential hermaphroditism (called dichogamy in
botany Botany, also called , plant biology or phytology, is the science of plant life and a branch of biology. A botanist, plant scientist or phytologist is a scientist who specialises in this field. The term "botany" comes from the Ancient Greek w ...
) is a type of
hermaphroditism In reproductive biology, a hermaphrodite () is an organism that has both kinds of reproductive organs and can produce both gametes associated with male and female sexes. Many taxonomic groups of animals (mostly invertebrates) do not have s ...
that occurs in many
fish Fish are aquatic, craniate, gill-bearing animals that lack limbs with digits. Included in this definition are the living hagfish, lampreys, and cartilaginous and bony fish as well as various extinct related groups. Approximately 95% of li ...
,
gastropod The gastropods (), commonly known as snails and slugs, belong to a large taxonomic class of invertebrates within the phylum Mollusca called Gastropoda (). This class comprises snails and slugs from saltwater, from freshwater, and from land. T ...
s, and plants. Sequential hermaphroditism occurs when the individual changes its sex at some point in its life. In particular, a sequential hermaphrodite produces eggs (female
gamete A gamete (; , ultimately ) is a haploid cell that fuses with another haploid cell during fertilization in organisms that reproduce sexually. Gametes are an organism's reproductive cells, also referred to as sex cells. In species that produce t ...
s) and sperm (male
gamete A gamete (; , ultimately ) is a haploid cell that fuses with another haploid cell during fertilization in organisms that reproduce sexually. Gametes are an organism's reproductive cells, also referred to as sex cells. In species that produce t ...
s) at different stages in life. Species that can undergo these changes from one sex to another do so as a normal event within their reproductive cycle that is usually cued by either social structure or the achievement of a certain age or size. In animals, the different types of change are male to female (protandry or protandrous hermaphroditism), female to male (protogyny or protogynous hermaphroditism), bidirectional (serial or bidirectional hermaphroditism). Both protogynous and protandrous hermaphroditism allow the organism to switch between functional male and functional female. Bidirectional hermaphrodites have the capacity for sex change in either direction between male and female or female and male, potentially repeatedly during their lifetime. These various types of sequential hermaphroditism may indicate that there is no advantage based on the original sex of an individual organism. Those that change gonadal sex can have both female and male germ cells in the
gonad A gonad, sex gland, or reproductive gland is a mixed gland that produces the gametes and sex hormones of an organism. Female reproductive cells are egg cells, and male reproductive cells are sperm. The male gonad, the testicle, produces sper ...
s or can change from one complete gonadal type to the other during their last life stage. In plants, individual flowers are called dichogamous if their function has the two sexes separated in time, although the plant as a whole may have functionally male and functionally female flowers open at any one moment. A flower is protogynous if its function is first female, then male, and protandrous if its function is male then female. It used to be thought that this reduced
inbreeding Inbreeding is the production of offspring from the mating or breeding of individuals or organisms that are closely related genetically. By analogy, the term is used in human reproduction, but more commonly refers to the genetic disorders and o ...
, but it may be a more general mechanism for reducing pollen-pistil interference.


Zoology

Teleost Teleostei (; Greek ''teleios'' "complete" + ''osteon'' "bone"), members of which are known as teleosts ), is, by far, the largest infraclass in the class Actinopterygii, the ray-finned fishes, containing 96% of all extant species of fish. Tel ...
fishes are the only vertebrate
lineage Lineage may refer to: Science * Lineage (anthropology), a group that can demonstrate its common descent from an apical ancestor or a direct line of descent from an ancestor * Lineage (evolution), a temporal sequence of individuals, populati ...
where sequential hermaphroditism occurs.


Protandry

In general, protandrous hermaphrodites are animals that develop as males, but can later reproduce as females. 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 hermaphrodite Simultaneous hermaphroditism is one of the two types of hermaphroditism, the other type being sequential hermaphroditism. In this form of hermaphroditism an individual has sex organs of both sexes and can produce both gamete types even in the sa ...
s), but shift their reproductive resources from male to female over time.


Protandrous examples

Protandry is uncommon, but does occur in a widespread range of animal phyla. In fact, protandrous hermaphroditism occurs in many fish,
mollusks Mollusca is the second-largest phylum of invertebrate animals after the Arthropoda, the members of which are known as molluscs or mollusks (). Around 85,000  extant species of molluscs are recognized. The number of fossil species is esti ...
, and
crustaceans Crustaceans (Crustacea, ) form a large, diverse arthropod taxon which includes such animals as decapods, seed shrimp, branchiopods, fish lice, krill, remipedes, isopods, barnacles, copepods, amphipods and mantis shrimp. The crustacean group ...
, but is completely absent in terrestrial vertebrates. Protandrous fishes include teleost species in the families Pomacentridae, Sparidae, and Gobiidae. A common example of a protandrous species are
clownfish Clownfish or anemonefish are fishes from the subfamily Amphiprioninae in the family Pomacentridae. Thirty species of clownfish are recognized: one in the genus '' Premnas'', while the remaining are in the genus '' Amphiprion''. In the wild, t ...
, which have a very structured society. In the ''
Amphiprion ''Amphiprion'' is a genus of ray-finned fish which comprises all but one of the species of clownfish or anemonefish in the subfamily Amphiprioninae of the family Pomacentridae. Species The following species are classified in the genus ''Amphipri ...
percula'' species, there are zero to four individuals excluded from breeding and a breeding pair living in a sea anemone. Dominance is based on size, the female being the largest and the reproductive male being the second largest. The rest of the group is made up of progressively smaller males that do not breed and have no functioning gonads. 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. Other protandrous fishes can be found in the classes
clupeiformes Clupeiformes is the order of ray-finned fish that includes the herring family, Clupeidae, and the anchovy family, Engraulidae. The group includes many of the most important forage and food fish. Clupeiformes are physostomes, which means that ...
,
siluriformes Catfish (or catfishes; order Siluriformes or Nematognathi) are a diverse group of ray-finned fish. Named for their prominent barbels, which resemble a cat's whiskers, catfish range in size and behavior from the three largest species alive, ...
, 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. Therefore, because other families also contain protandrous species, protandry likely has evolved multiple times. Other examples of protandrous animals include: * The Platyctenida order of comb jellies. Unlike most
ctenophores Ctenophora (; ctenophore ; ) comprise a phylum of marine invertebrates, commonly known as comb jellies, that inhabit sea waters worldwide. They are notable for the groups of cilia they use for swimming (commonly referred to as "combs"), a ...
, which are simultaneous hermaphrodites,
Platyctenida Platyctenida is an order of comb jellies. Taxonomy Platyctenida is the only benthic group of organisms in the phylum Ctenophora. Platyctenida are considered to be a phylogenetically young group along with the orders Lobata and Beroida and are ...
are primarily protandrous, but asexual reproduction has also been observed in some species. * The flatworms '' Hymanella retenuova''. *''
Laevapex fuscus ''Laevapex fuscus'', the dusky ancylid, is a species of small, freshwater, air-breathing limpet, an aquatic pulmonate gastropod mollusc or micromollusc in the family Planorbidae, the ram's horn snails and their allies. Geographic distrib ...
'', a
gastropod The gastropods (), commonly known as snails and slugs, belong to a large taxonomic class of invertebrates within the phylum Mollusca called Gastropoda (). This class comprises snails and slugs from saltwater, from freshwater, and from land. T ...
, is described as being functionally protandric. The
sperm Sperm is the male reproductive cell, or gamete, in anisogamous forms of sexual reproduction (forms in which there is a larger, female reproductive cell and a smaller, male one). Animals produce motile sperm with a tail known as a flagellum, whi ...
matures in late winter and early spring, the eggs mature in early summer, and
copulation Sexual intercourse (or coitus or copulation) is a sexual activity typically involving the insertion and thrusting of the penis into the vagina for sexual pleasure or reproduction.Sexual intercourse most commonly means penile–vaginal penetra ...
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 ''Speyeria mormonia,'' commonly known as the Mormon fritillary, is a North American butterfly belonging to the family Nymphalidae. It is highly diverse, having differentiated into several subspecies which occupy a wide geographic range. ''S. mor ...
'', or 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. *The shrimp genus ''
Lysmata ''Lysmata'' is a genus of shrimp in the infraorder Caridea, the caridean shrimp. The genus belongs to the family Lysmatidae. ''Lysmata'' are popular ornamental shrimp in the marine aquarium trade for their bright color patterns, interesting be ...
'' perform protandric simultaneous hermaphroditism where they become true hermaphrodites instead of females. During the "female phase," they have both male and female tissues in their gonads and produce both gametes.


Protogyny

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, especially when compared to protandry. As the animal ages, it shifts sex to become a male animal due to internal or external triggers. Unlike females, male
fecundity Fecundity is defined in two ways; in human demography, it is the potential for reproduction of a recorded population as opposed to a sole organism, while in population biology, it is considered similar to fertility, the natural capability to pr ...
increases greatly with age, and it is hypothesized that it is more selectively advantageous to be a male when an organism's body is larger. This advantage may cause certain species to be protogynous hermaphrodites as the sex change to male leads to an increased reproductive fitness advantage.


Protogynous examples

Protogyny is the most common form of hermaphroditism in fish in nature. 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 The wrasses are a family, Labridae, of marine fish, many of which are brightly colored. The family is large and diverse, with over 600 species in 81 genera, which are divided into 9 subgroups or tribes. They are typically small, most of them le ...
. 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. Large males hold territories and try to pair spawn, while small to mid-size initial-phase males live with females and group
spawn Spawn or spawning may refer to: * Spawn (biology), the eggs and sperm of aquatic animals Arts, entertainment, and media * Spawn (character), a fictional character in the comic series of the same name and in the associated franchise ** '' Spawn: ...
. 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 The California sheephead (''Semicossyphus pulcher'') is a species of wrasse native to the eastern Pacific Ocean. Its range is from Monterey Bay, California, to the Gulf of California, Mexico. It can live for up to 20 years in favorable condition ...
(''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 The oviduct in mammals, is the passageway from an ovary. In human females this is more usually known as the Fallopian tube or uterine tube. The eggs travel along the oviduct. These eggs will either be fertilized by spermatozoa to become a zygote, o ...
. 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 A testicle or testis (plural testes) is the male reproductive gland or gonad in all bilaterians, including humans. It is homologous to the female ovary. The functions of the testes are to produce both sperm and androgens, primarily testoster ...
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 ''Botryllus schlosseri'' is a colonial ascidian tunicate. It is commonly known as the star tunicate, but it also has several other common names, including star ascidian and golden star tunicate. Colonies grow on slow-moving, submerged objects, ...
'', a colonial
tunicate A tunicate is a marine invertebrate animal, a member of the subphylum Tunicata (). It is part of the Chordata, a phylum which includes all animals with dorsal nerve cords and notochords (including vertebrates). The subphylum was at one time ca ...
, 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%). Also a significantly lower percentage of larvae derived from self-fertilized eggs metamorphose, and the growth of the colonies derived from their metamorphosis is significantly lower. These findings suggest that self-fertilization gives rise to inbreeding depression associated with developmental deficits that are likely caused by expression of deleterious recessive mutations. Other examples of protogynous organisms include: * In the following
fish Fish are aquatic, craniate, gill-bearing animals that lack limbs with digits. Included in this definition are the living hagfish, lampreys, and cartilaginous and bony fish as well as various extinct related groups. Approximately 95% of li ...
families:
Serranidae The Serranidae are a large family of fishes belonging to the order Perciformes. The family contains about 450 species in 65 genera, including the sea basses and the groupers (subfamily Epinephelinae). Although many species are small, in some case ...
(groupers), Sparidae (porgies), Synbranchidae (swamp eels), Labridae (wrasses), Scaridae (parrotfishes),
Pomacanthidae Marine angelfish are perciform fish of the family Pomacanthidae. They are found on shallow reefs in the tropical Atlantic, Indian, and mostly western Pacific Oceans. The family contains seven genera and about 86 species. They should not be conf ...
(angelfishes),
Gobiidae Gobiidae or gobies is a family of bony fish in the order Gobiiformes, one of the largest fish families comprising more than 2,000 species in more than 200 genera. Most of gobiid fish are relatively small, typically less than in length, and the ...
(gobies), Lethrinidae (emperors), and possibly others. * The intertidal isopod Gnorimosphaeroma oregonense. * Protogyny sometimes occurs in the frog ''
Rana temporaria The common frog or grass frog (''Rana temporaria''), also known as the European common frog, European common brown frog, European grass frog, European Holarctic true frog, European pond frog or European brown frog, is a semi-aquatic amphibian ...
'', where older females will sometimes switch to being males.


Ultimate causes

The ultimate cause of a biological event determines how the event makes organisms better adapted to their environment, and thus why evolution by natural selection has produced that event. While a large number of ultimate causes of hermaphroditism have been proposed, the two causes most relevant to sequential hermaphroditism are the size-advantage model and protection against inbreeding.


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. In most
ectotherms An ectotherm (from the Greek () "outside" and () "heat") is an organism in which internal physiological sources of heat are of relatively small or of quite negligible importance in controlling body temperature.Davenport, John. Animal Life a ...
, body size and female fecundity are positively correlated. This supports the size-advantage model. Kazancioglu and Alonzo (2010) performed the first comparative analysis of sex change in Labridae. Their analysis supports the size-advantage model and suggest that sequential hermaphroditism is correlated to the size-advantage. They determined that
dioecy Dioecy (; ; adj. dioecious , ) is a characteristic of a species, meaning that it has distinct individual organisms (unisexual) that produce male or female gametes, either directly (in animals) or indirectly (in seed plants). Dioecious reproductio ...
was less likely to occur when the size advantage is stronger than other advantages. 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. An example of territoriality favoring protogyny occurs when there is a need to protect their habitat and being a large male is advantageous for this purpose. In the mating aspect, a large male has a higher chance of mating, while this has no effect on the female mating fitness. Thus, he suggests that female fecundity has more impact on sequential hermaphroditism than the age structures of the population. The size-advantage model predicts that sex change would only be absent if the relationship between size/age with reproductive potential is identical in both sexes. With this prediction one would assume that hermaphroditism is very common, but this is not the case. Sequential hermaphroditism is very rare and according to scientists this is due to some cost that decreases fitness in sex changers as opposed to those who don't change sex. Some of the hypotheses proposed for the dearth of hermaphrodites are the energetic cost of sex change, genetic and/or physiological barriers to sex change, and sex-specific mortality rates. 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.


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, and many examples of sequential hermaphroditism attributable to inbreeding prevention have been identified in a wide variety of animals.


Proximate causes

The
proximate cause In law and insurance, a proximate cause is an event sufficiently related to an injury that the courts deem the event to be the cause of that injury. There are two types of causation in the law: cause-in-fact, and proximate (or legal) cause. Ca ...
of a biological event concerns the molecular and physiological mechanisms that produce the event. Many studies have focused on the proximate causes of sequential hermaphroditism, which may be caused by various hormonal and enzyme changes in organisms. The role of
aromatase Aromatase (), also called estrogen synthetase or estrogen synthase, is an enzyme responsible for a key step in the biosynthesis of estrogens. It is CYP19A1, a member of the cytochrome P450 superfamily, which are monooxygenases that catalyze many ...
has been widely studied in this area. Aromatase is an
enzyme Enzymes () are proteins that act as biological catalysts by accelerating chemical reactions. The molecules upon which enzymes may act are called substrates, and the enzyme converts the substrates into different molecules known as products. A ...
that controls the
androgen An androgen (from Greek ''andr-'', the stem of the word meaning "man") is any natural or synthetic steroid hormone that regulates the development and maintenance of male characteristics in vertebrates by binding to androgen receptors. This in ...
/
estrogen Estrogen or oestrogen is a category of sex hormone responsible for the development and regulation of the female reproductive system and secondary sex characteristics. There are three major endogenous estrogens that have estrogenic hormonal acti ...
ratio in animals by catalyzing the conversion of
testosterone Testosterone is the primary sex hormone and anabolic steroid in males. In humans, testosterone plays a key role in the development of Male reproductive system, male reproductive tissues such as testes and prostate, as well as promoting secondar ...
into
oestradiol Estradiol (E2), also spelled oestradiol, is an estrogen steroid hormone and the major female sex hormone. It is involved in the regulation of the estrous and menstrual female reproductive cycles. Estradiol is responsible for the development of f ...
, which is irreversible. It has been discovered that the aromatase pathway mediates sex change in both directions in organisms. 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 gonodal 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 Teleostei (; Greek ''teleios'' "complete" + ''osteon'' "bone"), members of which are known as teleosts ), is, by far, the largest infraclass in the class Actinopterygii, the ray-finned fishes, containing 96% of all extant species of fish. Tel ...
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
metalloproteinase A metalloproteinase, or metalloprotease, is any protease enzyme whose catalytic mechanism involves a metal. An example is ADAM12 which plays a significant role in the fusion of muscle cells during embryo development, in a process known as myo ...
s (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 cell Leydig cells, also known as interstitial cells of the testes and interstitial cells of Leydig, are found adjacent to the seminiferous tubules in the testicle and produce testosterone in the presence of luteinizing hormone (LH). They are polyhedral ...
s 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 The effective population size (''N'e'') is a number that, in some simplified scenarios, corresponds to the number of breeding individuals in the population. More generally, ''N'e'' is the number of individuals that an idealised population w ...
(Ne). However, a study of two ecologically similar santer sea bream (
gonochoric In biology, gonochorism is a sexual system where there are only two sexes and each individual organism is either male or female. The term gonochorism is usually applied in animal species, the vast majority of which are gonochoric. Gonochorism c ...
) 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

Sequential hermaphroditism in plants is the process in which a plant changes its sex throughout its lifetime. Sequential hermaphroditism in plants is very rare. There are less than 0.1% of recorded cases in which plant species entirely change their sex. The Patchy Environment Model and Size Dependent Sex Allocation are the two environmental factors which drive sequential hermaphroditism in plants. The Patchy Environment Model states that plants will want to maximize the use of their resources through the change of their sex. For example, if a plant will benefit more from the resources of a given environment in a certain sex, it will want to change to that sex. Furthermore, Size Dependent Sex Allocation outlines that in sequential hermaphroditic plants, it is preferable to change sexes in a way that maximizes their overall fitness compared to their size over time. Similar to maximizing the use of resources, if the combination of size and fitness for a certain sex is more beneficial, the plant will want to change to that sex. Evolutionarily, sequential
hermaphrodite In reproductive biology, a hermaphrodite () is an organism that has both kinds of reproductive organs and can produce both gametes associated with male and female sexes. Many Taxonomy (biology), taxonomic groups of animals (mostly invertebrate ...
s emerged as certain species found that one of the best ways to maximize the benefits of their environment was through changing their sex.


Arisaema

''
Arisaema ''Arisaema'' is a large and diverse genus of the flowering plant family Araceae. The largest concentration of species is in China and Japan, with other species native to other parts of southern Asia as well as eastern and central Africa, Mexico ...
'' is a plant genus which is commonly cited as exercising sequential hermaphroditism. The most commonly known ''Arisaema'' plant is ''
Arisaema triphyllum ''Arisaema triphyllum'', the jack-in-the-pulpit, bog onion, brown dragon or Indian turnip, is a herbaceous perennial plant growing from a corm. It is a highly variable species typically growing in height with three-part leaves and flowers conta ...
'' (Jack in the pulpit) plant. As the ''A. triphyllum'' grows and changes, it develops from a nonsexual juvenile plant, to a young all-male plant, to a male-and-female plant, to an all-female plant. This means that ''A. triphyllum'' is changing its sex from male to female over the course of its lifetime as its size increases, showcasing Size Dependent Sex Allocation. Another example is '' Arisaema dracontium'' or the green dragon, which can change its sex on a yearly basis. ''A. dracontiums sex is also dependent on size: the smaller flowers are male while the larger flowers are both male and female. Typically in ''Arisaema'' species, small flowers only contain stamens, meaning they are males. Larger flowers can contain both stamen and pistils or only pistils, meaning they can be either hermaphrodites or strictly female. Overall, ''Arisaemas'' are changing their sex as they grow larger, maximizing the overall fitness for that particular environment.


Striped maple (''Acer pensylvanicum'')

Striped maple trees ('' Acer pensylvanicum'') are sequential hermaphrodites as they are known to have the ability to change sex. Starting in 2014, a case study showed that over a four year time span 54% of striped maple trees developed a different sex. Scientists removed branches from striped maple trees to research the cause of their sequential hermaphroditism. It was found that the branches changed to either female or female and male as a response to being damaged by being cut off the tree. Researchers concur that when the striped maple experiences damage or is sick, this will trigger a sex change to either female or female and male. This could be because the striped maple would need to bloom as quickly as possible, producing offspring before it ultimately dies from damage or sickness.


Dichogamy in flowering plants

In the context of the
plant sexuality Plant reproductive morphology is the study of the physical form and structure (the morphology) of those parts of plants directly or indirectly concerned with sexual reproduction. Among all living organisms, flowers, which are the reproductive s ...
of flowering plants (angiosperms), there are two forms of dichogamy: ''protogyny''—female function precedes male function—and ''protandry''—male function precedes female function. Examples include in
Asteraceae The family Asteraceae, alternatively Compositae, consists of over 32,000 known species of flowering plants in over 1,900 genera within the order Asterales. Commonly referred to as the aster, daisy, composite, or sunflower family, Compositae w ...
, bisexual tubular (disks) florets are usually protandrous. Whereas in ''
Acacia ''Acacia'', commonly known as the wattles or acacias, is a large genus of shrubs and trees in the subfamily Mimosoideae of the pea family Fabaceae. Initially, it comprised a group of plant species native to Africa and Australasia. The genus na ...
'' and ''
Banksia ''Banksia'' is a genus of around 170 species in the plant family Proteaceae. These Australian wildflowers and popular garden plants are easily recognised by their characteristic flower spikes, and fruiting "cones" and heads. ''Banksias'' range ...
'' flowers are protogynous, with the style of the female flower elongating, then in the male phase shedding pollen.


Evolution

Historically, dichogamy has been regarded as a mechanism for reducing
inbreeding Inbreeding is the production of offspring from the mating or breeding of individuals or organisms that are closely related genetically. By analogy, the term is used in human reproduction, but more commonly refers to the genetic disorders and o ...
. However, a survey of the angiosperms found that
self-incompatible Self-incompatibility (SI) is a general name for several genetic mechanisms that prevent self-fertilization in sexually reproducing organisms, and thus encourage outcrossing and allogamy. It is contrasted with separation of sexes among individuals ...
(SI) plants, which are incapable of inbreeding, were as likely to be dichogamous as were self-compatible (SC) plants. This finding led to a reinterpretation of dichogamy as a more general mechanism for reducing the impact of
pollen Pollen is a powdery substance produced by seed plants. It consists of pollen grains (highly reduced microgametophytes), which produce male gametes (sperm cells). Pollen grains have a hard coat made of sporopollenin that protects the gametophyt ...
-
pistil Gynoecium (; ) is most commonly used as a collective term for the parts of a flower that produce ovules and ultimately develop into the fruit and seeds. The gynoecium is the innermost whorl of a flower; it consists of (one or more) ''pistils'' ...
interference on pollen import and export. Unlike the
inbreeding avoidance Inbreeding avoidance, or the inbreeding avoidance hypothesis, is a concept in evolutionary biology that refers to the prevention of the deleterious effects of inbreeding. Animals only rarely exhibit inbreeding avoidance. The inbreeding avoidance ...
hypothesis, which focused on female function, this interference-avoidance hypothesis considers both reproductive functions.


Mechanism

In many hermaphroditic species, the close physical proximity of
anthers The stamen (plural ''stamina'' or ''stamens'') is the pollen-producing reproductive organ of a flower. Collectively the stamens form the androecium., p. 10 Morphology and terminology A stamen typically consists of a stalk called the filam ...
and stigma makes interference unavoidable, either within a
flower A flower, sometimes known as a bloom or blossom, is the reproductive structure found in flowering plants (plants of the division Angiospermae). The biological function of a flower is to facilitate reproduction, usually by providing a mechani ...
or between flowers on an
inflorescence An inflorescence is a group or cluster of flowers arranged on a stem that is composed of a main branch or a complicated arrangement of branches. Morphologically, it is the modified part of the shoot of seed plants where flowers are formed o ...
. Within-flower interference, which occurs when either the pistil interrupts pollen removal or the anthers prevent pollen deposition, can result in autonomous or facilitated self-pollination. Between-flower interference results from similar mechanisms, except that the interfering structures occur on different flowers within the same inflorescence and it requires
pollinator A pollinator is an animal that moves pollen from the male anther of a flower to the female stigma of a flower. This helps to bring about fertilization of the ovules in the flower by the male gametes from the pollen grains. Insects are the maj ...
activity. This results in geitonogamous pollination, the transfer of pollen between flowers of the same individual. In contrast to within-flower interference, geitonogamy necessarily involves the same processes as outcrossing: pollinator attraction, reward provisioning, and pollen removal. Therefore, between-flower interference not only carries the cost of self-fertilization (
inbreeding depression Inbreeding depression is the reduced biological fitness which has the potential to result from inbreeding (the breeding of related individuals). Biological fitness refers to an organism's ability to survive and perpetuate its genetic material. In ...
), but also reduces the amount of pollen available for export (so-called "pollen discounting"). Because pollen discounting diminishes outcross siring success, interference avoidance may be an important evolutionary force in floral biology. Dichogamy may reduce between-flower interference by reducing or eliminating the temporal overlap between stigma and anthers within an inflorescence. Large inflorescences attract more pollinators, potentially enhancing reproductive success by increasing pollen import and export. However, large inflorescences also increase the opportunities for both geitonogamy and pollen discounting, so that the opportunity for between-flower interference increases with inflorescence size. Consequently, the evolution of floral display size may represent a compromise between maximizing pollinator visitation and minimizing geitonogamy and pollen discounting (Barrett et al., 1994).


Protandry

Protandry may be particularly relevant to this compromise, because it often results in an inflorescence structure with female phase flowers positioned below male phase flowers. Given the tendency of many insect pollinators to forage upwards through inflorescences, protandry may enhance pollen export by reducing between-flower interference. Furthermore, this enhanced pollen export should increase as floral display size increases, because between-flower interference should increase with floral display size. These effects of protandry on between-flower interference may decouple the benefits of large inflorescences from the consequences of geitonogamy and pollen discounting. Such a decoupling would provide a significant reproductive advantage through increased pollinator visitation and siring success.


Advantages

Harder et al. (2000) demonstrated experimentally that dichogamy both reduced rates of self-fertilization and enhanced outcross siring success through reductions in geitonogamy and pollen discounting, respectively. Routley & Husband (2003) examined the influence of inflorescence size on this siring advantage and found a bimodal distribution with increased siring success with both small and large display sizes. The length of stigmatic receptivity plays a key role in regulating the isolation of the male and female stages in dichogamous plants, and stigmatic receptivity can be influenced by both temperature and humidity. Another study by Jersakova and Johnson, studied the effects of protandry on the pollination process of the moth pollinated orchid, ''Satyrium longicauda''. They discovered that protandry tended to reduce the absolute levels of self-pollination and suggest that the evolution of protandry could be driven by the consequences of the pollination process for male mating success. Another study that indicated that dichogamy might increase male pollination success was by Dai and Galloway.


See also

*
Plant sexuality Plant reproductive morphology is the study of the physical form and structure (the morphology) of those parts of plants directly or indirectly concerned with sexual reproduction. Among all living organisms, flowers, which are the reproductive s ...
*
Sequential hermaphrodite Sequential hermaphroditism (called dichogamy in botany) is a type of hermaphroditism that occurs in many fish, gastropods, and plants. Sequential hermaphroditism occurs when the individual changes its sex at some point in its life. In particular, ...
section in
Hermaphrodite In reproductive biology, a hermaphrodite () is an organism that has both kinds of reproductive organs and can produce both gametes associated with male and female sexes. Many Taxonomy (biology), taxonomic groups of animals (mostly invertebrate ...


References

{{Reflist, 30em Reproduction Pollination Sexual system