Sequential hermaphroditism
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Sequential hermaphroditism (called dichogamy in
In animals, the different types of change are male to female (protandry or protandrous hermaphroditism), female to male (protogyny or protogynous hermaphroditism),[5] and bidirectional (serial or bidirectional hermaphroditism).[6] Both protogynous and protandrous hermaphroditism allow the organism to switch between functional male and functional female.[7] Bidirectional hermaphrodites have the capacity for sex change in either direction between male and female or female and male, potentially repeatedly during their lifetime.[6] These various types of sequential hermaphroditism may indicate that there is no advantage based on the original sex of an individual organism.[7] Those that change gonadal sex can have both female and male germ cells in the gonads or can change from one complete gonadal type to the other during their last life stage.[8]
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,[9] but it may be a more general mechanism for reducing pollen-pistil interference.[10]
Zoology
Teleost fishes are the only vertebrate lineage where sequential hermaphroditism occurs.[3]
Protandry
In general, protandrous hermaphrodites are animals that develop as males, but can later reproduce as females.[11] 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.[12]
Furthermore, there are also species that reproduce as both sexes throughout their lifespans (i.e
Protandrous examples
Protandry occurs in a widespread range of animal phyla.
Protandrous fishes include teleost species in the families
Other protandrous fishes can be found in the classes
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.[17] 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, which are simultaneous hermaphrodites, Platyctenida are primarily protandrous, but asexual reproduction has also been observed in some species.[21]
- The flatworms Hymanella retenuova.[22]
- 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.[23][24]
- Speyeria mormonia, 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.[25]
- The shrimp genus Lysmata perform protandric simultaneous hermaphroditism where they become true hermaphrodites instead of females.[16] During the "female phase," they have both male and female tissues in their gonads and produce both gametes.[26]
Protogyny
Protogynous hermaphrodites are animals that are born female and at some point in their lifespan change sex to male.[27] Protogyny is a more common form of sequential hermaphroditism in fish, especially when compared to protandry.[28] As the animal ages, it shifts sex to become a male animal due to internal or external triggers, undergoing phyiological and behavioral changes.[29] 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.[27][17]
Protogynous examples
Protogyny is the most common form of hermaphroditism in fish in nature.[30] About 75% of the 500 known sequentially hermaphroditic fish species are protogynous and often have polygynous mating systems.[31][32] 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.[33] 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
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.[37] 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[35] since all California sheephead are born female.[38]
Botryllus schlosseri, a colonial tunicate, is a protogynous hermaphrodite. In a colony, eggs are released about two days before the peak of sperm emission.[41] 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%).[41] 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.[42]
Other examples of protogynous organisms include:
- In the following Scaridae (parrotfishes),[48] Pomacanthidae (angelfishes),[49] Gobiidae (gobies),[50] Lethrinidae (emperors),[51] and possibly others.[52]
- The intertidal isopod Gnorimosphaeroma oregonense.[53]
- Protogyny sometimes occurs in the frog Rana temporaria, where older females will sometimes switch to being males.[23]
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[27] and protection against inbreeding.[54]
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.[54]
In most
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 do not 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.[5][56][57]
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.[58]
The size-advantage model also explains under which mating systems protogyny or protandry would be more adaptive.[54][59] In a haremic mating system, with one large male controlling access to numerous females for mating, this large male acheives greater reprodcutive success than a small female as he can fertilize numerous baches 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,[2] and many examples of sequential hermaphroditism attributable to inbreeding prevention have been identified in a wide variety of animals.[54]
Proximate causes
The proximate cause 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
Previous studies have also investigated sex reversal mechanisms in
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
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.[65] 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.[66] 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 hermaphrodites 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 is a plant genus which is commonly cited as exercising sequential hermaphroditism. The most commonly known Arisaema plant is Arisaema triphyllum (Jack in the pulpit) plant.[67][68] 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.[67] A. dracontium's 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.[67] 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.[69] Scientists removed branches from striped maple trees to research the cause of their sequential hermaphroditism.[70] 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
Evolution
Historically, dichogamy has been regarded as a mechanism for reducing
Unlike 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
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.[88] Given the tendency of many insect pollinators to forage upwards through inflorescences,[89] protandry may enhance pollen export by reducing between-flower interference.[90][9] 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.[90] 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.[91]
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.[92] 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.[93] Another study that indicated that dichogamy might increase male pollination success was by Dai and Galloway.[94]
See also
- Plant sexuality
- Sequential hermaphrodite section in Hermaphrodite
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