Gynodioecy

Last updated April 14, 2024

Lobelia siphilitica is an example of a species with a gynodioecious mating system. Lobelia-siphilitica-2014-08-30-Cranberry-03.jpg — *Lobelia siphilitica* is an example of a species with a gynodioecious mating system.

Gynodioecy is a rare breeding system that is found in certain flowering plant species in which female and hermaphroditic plants coexist within a population. Gynodioecy is the evolutionary intermediate between hermaphroditism (exhibiting both female and male parts) and dioecy (having two distinct morphs: male and female).

Gynodioecy occurs as a result of a genetic mutation that inhibits a hermaphroditic plant from producing pollen, while keeping the female reproductive parts intact. Gynodioecy is extremely rare, with fewer than 1% of angiosperm species exhibiting the breeding system. Some notable taxa that exhibit a gynodioecious mating system include Beta vulgaris (wild beet), Lobelia siphilitica , Silene , and Lamiaceae.

Evolution

Gynodioecy is often referred to as the evolutionary intermediate state between hermaphroditism and dioecy, however there is no evidence it is an intermediate state in animals.^[3] Gynodioecy has been investigated by biologists dating as far back as to Charles Darwin.^[4]

Gynodioecy can evolve from hermaphroditism due to certain environmental factors. If enough resources in a population are allocated to the female functions in a hermaphroditic species, gynodioecy will ensue. On the other hand, if more of those resources favor a hermaphrodite's male functions, androdioecy will result. A high rate of self-pollination in a population facilitates the maintenance of gynodioecy by increasing the inbreeding costs for hermaphrodites.^[5] Thus, as the rate of inbreeding increases in a population, the more likely gynodioecy is to occur.

Hermaphroditic plants may be able to reproduce on their own but in many species they are self-incompatible.^[6] Research has shown that a species can be either gynodioecious or self-incompatible, but very rarely is there a co-occurrence between the two. Therefore, gynodioecy and self-incompatibility tend to prevent each other's maintenance. Self-incompatibility of plants helps maintain androdioecy in plants, since males are in competition with only hermaphrodites to fertilize ovules. Self-incompatibility leads to a loss in gynodioecy, since neither hermaphrodites nor females have to deal with inbreeding depression.^[7]

Two scenarios have been proposed to explain the evolutionary dynamics of the maintenance of gynodioecy. The first scenario, known as the balancing selection theory, considers the genetic factors that control gynodioecy over long evolutionary time scales. The balancing selection leads to cycles that explain the normal sex ratios in gynodioecious populations. The second scenario, known as epidemic dynamics, involves the arrival and loss of new cytoplasmic male sterility genes in new populations. These are the same genes that invade hermaphrodite populations and eventually result in gynodioecy.^[4]

Mechanism

Gynodioecy is determined as a result of a genetic mutation that stops a plant from producing pollen, but still allows normal female reproductive features.^[8] In plants, nuclear genes are inherited from both parents, but all the cytoplasmic genes come from the mother. This allows male gametes to be smaller and more motile while female gametes are larger. It makes sense for most plants to be hermaphrodites, since they are sessile and unable to find mates as easily as animals can.^[9]

Cytoplasmic male sterility genes, usually found in the mitochondrial genome, show up and are established when female fertility is just slightly more than the hermaphroditic fertility. The female only needs to make slightly more or better seeds than hermaphrodites since the mitochondrial genome is maternally inherited.^[10] Research done on plants has shown that hermaphroditic plants are in constant battles against organelle genes trying to kill their male parts. In over 140 plant species, these “male killer” genes have been observed. Male sterility genes cause plants to grow anthers that are stunted or withered and as a result, do not produce pollen. In most plants, there are nuclear fertility restoring genes that counteract the work of the male sterility genes, maintaining the hermaphroditic state of the plant. However, in some species of plants, the male sterility genes win the battle over the nuclear fertility restoring genes, and gynodioecy occurs.^[9]

Maize farmers take advantage of gynodioecy to produce favorable hybrid maize seeds. The farmers deliberately make use of the gynodioecy that develops in the maize, resulting in a population of male-sterile and female-fertile individuals. They then introduce a new strain of male-sterile individuals and the breeders are able to collect the more favorable hybrid seeds.^[9]

Species distribution

Gynodioecy is a rare, but widely distributed sexual system in angiosperm species. Gynodioecy is found in at least 81 different angiosperm families but less than 1% of the angiosperms species on Earth are gynodioecious.^[11] One likely explanation for its rarity is due to its limited evolution. Since females are at a disadvantage when compared with hermaphrodites, they will never be able to evolve as quickly. In addition, gynodioecy is rare because the mechanisms that favor females and cause gynodioecy in some populations only operate in some plant lineages, but not others.

The reason for this variation in the rarity of gynodioecy stems from certain phenotypic traits or ecological factors that promote and favor the presence of female plants in a population. For example, a herbaceous growth form is much more highly favored in gynodioecious species of Lamiaceae when compared with woody lineages.^[11] Herbaceous growth form is also associated with a reduced pollen limitation^{[ clarification needed ]} and increased self-fertilization. A reduced pollen limitation may decrease seed quantity and quality. Woody growth form Lamiaceae are more pollen-limited and thus produce fewer seeds and seeds of lower quality, thus favoring the female herbaceous growth form.^[11] Gynodioecy is rare because some sexual systems are more evolutionarily liable to change in certain lineages in comparison with others.^{[ citation needed ]}

It has been estimated that gynodioecy occurs in 13.3% of Silene species.^[12]

Maintenance

Theoretically, hermaphrodites should have the evolutionary and reproductive advantage over females in a population because they naturally can produce more offspring. Hermaphrodites can transmit their genes through both pollen and ovules, whereas females can only transmit genes via ovules. Thus, in order for females to remain viable in a population, they would have to be twice as successful as hermaphrodites.

It would appear that gynodioecy should not persist. In order for it to be maintained, the females need to have some sort of a reproductive advantage over the hermaphroditic population, known as female compensation or female advantage.^[4] Female advantage includes an increase in saved energy from not producing pollen and making seedlings of higher quality, since hermaphrodite seedlings are susceptible to homozygous deleterious alleles. Additional advantages include more flowers, higher fruit set, higher total seed production, heavier seeds, and better germination rates.

Inbreeding depression

Inbreeding depression was found to be an important factor in the maintenance of gynodioecy in an endemic Hawaiian shrub Schiedea adamantis occurring in a single population in Diamond Head Crater Oahu.^[13] Inbreeding depression, due to selfing in the hermaphrodites, was considered to be caused by the presence of many mutations of small effect.^[13]

Examples

The following species and higher taxa have been observed to exhibit a gynodioecious breeding system:

Related Research Articles

Sex is the trait that determines whether a sexually reproducing organism produces male or female gametes. During sexual reproduction, a male and a female gamete fuse to form a zygote, which develops into an offspring that inherits traits from each parent. By convention, organisms that produce smaller, more mobile gametes are called male, while organisms that produce produce larger, non-mobile gametes are called female. An organism that produces both types of gamete is hermaphrodite.

Silene is a genus of flowering plants in the family Caryophyllaceae. Containing nearly 900 species, it is the largest genus in the family. Common names include campion and catchfly. Many Silene species are widely distributed, particularly in the northern hemisphere.

Plant reproductive morphology is the study of the physical form and structure of those parts of plants directly or indirectly concerned with sexual reproduction.

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 (dioecy), and their various modes of spatial (herkogamy) and temporal (dichogamy) separation.

In biology, gonochorism is a sexual system where there are 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.

Dioecy is a characteristic of certain species that have distinct unisexual individuals, each producing either male or female gametes, either directly or indirectly. Dioecious reproduction is biparental reproduction. Dioecy has costs, since only the female part of the population directly produces offspring. It is one method for excluding self-fertilization and promoting allogamy (outcrossing), and thus tends to reduce the expression of recessive deleterious mutations present in a population. Plants have several other methods of preventing self-fertilization including, for example, dichogamy, herkogamy, and self-incompatibility.

Sequential hermaphroditism is one of the two types of hermaphroditism, the other type being simultaneous hermaphroditism. It occurs when the organism's sex changes at some point in its life. In particular, a sequential hermaphrodite produces eggs and sperm at different stages in life. Sequential hermaphroditism occurs in many fish, gastropods, and plants. Species that can undergo these changes do so as a normal event within their reproductive cycle, usually cued by either social structure or the achievement of a certain age or size. In some species of fish, sequential hermaphroditism is much more common than simultaneous hermaphroditism.

Allogamy or cross-fertilization is the fertilization of an ovum from one individual with the spermatozoa of another. By contrast, autogamy is the term used for self-fertilization. In humans, the fertilization event is an instance of allogamy. Self-fertilization occurs in hermaphroditic organisms where the two gametes fused in fertilization come from the same individual. This is common in plants and certain protozoans.

The mechanisms of reproductive isolation are a collection of evolutionary mechanisms, behaviors and physiological processes critical for speciation. They prevent members of different species from producing offspring, or ensure that any offspring are sterile. These barriers maintain the integrity of a species by reducing gene flow between related species.

Cytoplasmic male sterility is total or partial male sterility in hermaphrodite organisms, as the result of specific nuclear and mitochondrial interactions. Male sterility is the failure to produce functional anthers, pollen, or male gametes. Such male sterility in hermaphrodite populations leads to gynodioecious populations.

Sex chromosomes are chromosomes that carry the genes that determine the sex of an individual. The human sex chromosomes are a typical pair of mammal allosomes. They differ from autosomes in form, size, and behavior. Whereas autosomes occur in homologous pairs whose members have the same form in a diploid cell, members of an allosome pair may differ from one another.

Androdioecy is a reproductive system characterized by the coexistence of males and hermaphrodites. Androdioecy is rare in comparison with the other major reproductive systems: dioecy, gynodioecy and hermaphroditism. In animals, androdioecy has been considered a stepping stone in the transition from dioecy to hermaphroditism, and vice versa.

A hermaphrodite is a sexually reproducing organism that produces both male and female gametes. Animal species in which individuals are of different sexes, either male or female but not both, are gonochoric, which is the opposite of hermaphroditic.

Teucrium racemosum, also commonly referred to as either the grey germander or forest germander, is a species of flowering plant in the family Lamiaceae. It is endemic to Australia and is found in all mainland states, the Northern Territory and the Australian Capital Territory. It grows in floodplains, dry lake beds and open woodlands. A perennial herb, it has four-sided, densely hairy stems, narrow egg-shaped leaves, and white flowers usually arranged singly in leaf axils. It grows to be between 15 and 40 cm tall.

Silene is a flowering plant genus that has evolved a dioecious reproductive system. This is made possible through heteromorphic sex chromosomes expressed as XY. Silene recently evolved sex chromosomes 5-10 million years ago and are widely used by geneticists and biologists to study the mechanisms of sex determination since they are one of only 39 species across 14 families of angiosperm that possess sex-determining genes. Silene are studied because of their ability to produce offspring with a plethora of reproductive systems. The common inference drawn from such studies is that the sex of the offspring is determined by the Y chromosome.

Trioecy, tridioecy or subdioecy, is a sexual system characterized by the coexistence of males, females, and hermaphrodites. It has been found in both plants and animals. Trioecy, androdioecy and gynodioecy may be described as mixed mating systems.

Andromonoecy is a breeding system of plant species in which male and hermaphrodite flowers are on the same plant. It is a monomorphic sexual system comparable with monoecy, gynomonoecy and trimonoecy. Andromonoecy is frequent among genera with zygomorphic flowers, however it is overall rare and occurs in less than 2% of plant species. Nonetheless the breeding system has gained interest among biologists in the study of sex expression.

Gynomonoecy is defined as the presence of both female and hermaphrodite flowers on the same individual of a plant species. It is prevalent in Asteraceae but is poorly understood.

Monoecy is a sexual system in seed plants where separate male and female cones or flowers are present on the same plant. It is a monomorphic sexual system comparable with gynomonoecy, andromonoecy and trimonoecy, and contrasted with dioecy where individual plants produce cones or flowers of only one sex and with bisexual or hermaphroditic plants in which male and female gametes are produced in the same flower.

A sexual system is a pattern of sex allocation or a distribution of male and female function across organisms in a species. Terms like reproductive system and mating system have also been used as synonyms.

References

↑ Fusco G, Minelli A (2019-10-10). The Biology of Reproduction. Cambridge University Press. p. 134. ISBN 978-1-108-49985-9.
↑ Torices, Rubén; Méndez, Marcos; Gómez, José María (2011). "Where do monomorphic sexual systems fit in the evolution of dioecy? Insights from the largest family of angiosperms". New Phytologist. 190 (1): 234–248. doi: 10.1111/j.1469-8137.2010.03609.x . ISSN 1469-8137. PMID 21219336.
↑ Leonard JL (October 2013). "Williams' paradox and the role of phenotypic plasticity in sexual systems". Integrative and Comparative Biology. 53 (4): 671–88. doi: 10.1093/icb/ict088 . PMID 23970358.
1 2 3 Touzet P (2012). "Mitochondrial genome evolution and gynodioecy". In Marechal-Drouard L (ed.). Mitochondrial genome evolution. Advances in botanical research. Academic Press. pp. 71–98. ISBN 9780123944429.
↑ Sinclair JP, Kameyama Y, Shibata A, Kudo G (September 2016). "Male-biased hermaphrodites in a gynodioecious shrub, Daphne jezoensis". Plant Biology. 18 (5): 859–67. doi:10.1111/plb.12463. PMID 27090773.
↑ Takayama S, Isogai A (January 2003). "Molecular mechanism of self-recognition in Brassica self-incompatibility". Journal of Experimental Botany. 54 (380): 149–56. doi: 10.1093/jxb/erg007 . PMID 12456765.
↑ Van de Paer C, Saumitou-Laprade P, Vernet P, Billiard S (April 2015). "The joint evolution and maintenance of self-incompatibility with gynodioecy or androdioecy". Journal of Theoretical Biology. 371: 90–101. doi:10.1016/j.jtbi.2015.02.003. PMID 25681148.
↑ Preece T, Mao Y (September 2010). "The evolution of gynodioecy on a lattice" (PDF). Journal of Theoretical Biology. 266 (2): 219–25. Bibcode:2010JThBi.266..219P. doi:10.1016/j.jtbi.2010.06.025. PMID 20599548. S2CID 8526610.
1 2 3 Ridley M (1993). The red queen: sex and the evolution of human nature. Penguin. pp. 91–128. ISBN 978-0140167726.
↑ Delph LF, Touzet P, Bailey MF (January 2007). "Merging theory and mechanism in studies of gynodioecy". Trends in Ecology & Evolution. 22 (1): 17–24. doi:10.1016/j.tree.2006.09.013. PMID 17028054.
1 2 3 Rivkin LR, Case AL, Caruso CM (July 2016). "Why is gynodioecy a rare but widely distributed sexual system? Lessons from the Lamiaceae". The New Phytologist. 211 (2): 688–96. doi: 10.1111/nph.13926 . PMID 26991013.
↑ Casimiro-Soriguer I, Buide ML, Narbona E (April 2015). "Diversity of sexual systems within different lineages of the genus Silene". AoB Plants. 7. doi:10.1093/aobpla/plv037. PMC 4433491 . PMID 25862920.
1 2 Sakai AK, Weller SG, Chen ML, Chou SY, Tasanont C. Evolution of gynodioecy and maintenance of females: The role of inbreeding depression, outcrossing rates, and resource allocation in Schiedea adamantis (Caryophyllaceae). Evolution. 1997 Jun;51(3):724-736. doi: 10.1111/j.1558-5646.1997.tb03656.x. PMID: 28568572
↑ Wise M, Vu J, Carr D (2011). "Potential Ecological Constraints on the Evolution of Gynodioecy in Mimulus guttatus: Relative Fecundity and Pollinator Behavior in a Mixed-Sex Population". International Journal of Plant Sciences. 172 (2): 199–210. doi:10.1086/657677. JSTOR 10.1086/657677. S2CID 84827182 . Retrieved 24 June 2021.