Lobelia-siphilitica-2014-08-30-Cranberry-03

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 A hermaphrodite () is a sexually reproducing organism that produces both male and female gametes. Animal species in which individuals are either male or female are gonochoric, which is the opposite of hermaphroditic. The individuals of many ...

(exhibiting both female and male parts) and

dioecy Dioecy ( ; ; adj. dioecious, ) is a characteristic of certain species that have distinct unisexual individuals, each producing either male or female gametes, either directly (in animals) or indirectly (in seed plants). Dioecious reproduction is ...

(having two distinct morphs: male and female). Gynodioecy is sometimes considered a mixed mating system comparable with

trioecy Trioecy , also spelled triecy, is a sexual system characterized by the coexistence of males, females, and hermaphrodites. It has been found in both plants and animals. Like androdioecy and gynodioecy, trioecy is a mixed mating systems. Term ...

and

androdioecy 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 ...

. It is also considered a dimorphic sexual system alongside

and

. Gynodioecy occurs as a result of transmission of nuclear (nuclear male sterility) or, more commonly, extra-nuclear (e.g.

cytoplasmic male sterility 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 m ...

) mutated alleles, which prevents pollen production, while keeping the female reproductive parts intact; other members of the species population don't inherit the mutated alleles, thus remaining hermaphrodites. In some cases, a combination of both nuclear and extra-nuclear mechanisms is observed in determining the sterile phenotype. 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 ''Beta vulgaris'' (beet) is a species of flowering plant in the subfamily Betoideae of the family Amaranthaceae. Economically, it is the most important crop of the large order Caryophyllales. It has several cultivar groups: the sugar beet, of gre ...

'' (wild beet), ''

Lobelia siphilitica ''Lobelia siphilitica'', the great blue lobelia, great lobelia, or blue cardinal flower, is a plant species within the family Campanulaceae. It is an herbaceous perennial dicot native to eastern and central Canada and United States. There are two ...

'', ''

Silene ''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, particularl ...

'', and

Lamiaceae The Lamiaceae ( ) or Labiatae are a family (biology), family of flowering plants commonly known as the mint, deadnettle, or sage family. Many of the plants are aromatic in all parts and include widely used culinary herbs like basil (herb), ba ...

Etymology

The word gynodioecy comes from

Greek Greek may refer to: Anything of, from, or related to Greece, a country in Southern Europe: *Greeks, an ethnic group *Greek language, a branch of the Indo-European language family **Proto-Greek language, the assumed last common ancestor of all kno ...

; ''gyne'' (woman), ''di'' (twice or double), and ''okios'' (house). The term was first used by

Charles Darwin Charles Robert Darwin ( ; 12 February 1809 – 19 April 1882) was an English Natural history#Before 1900, naturalist, geologist, and biologist, widely known for his contributions to evolutionary biology. His proposition that all speci ...

in 1877 when writing about

plant morphology Phytomorphology is the study of the physical form and external structure of plants.Raven, P. H., R. F. Evert, & S. E. Eichhorn. ''Biology of Plants'', 7th ed., page 9. (New York: W. H. Freeman, 2005). . This is usually considered distinct from pl ...

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. Gynodioecy has been investigated by biologists dating as far back as to

. 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,

will result. A high rate of

self-pollination Self-pollination is a form of pollination in which pollen arrives at the stigma of a flower (in flowering plants) or at the ovule (in gymnosperms) of the same plant. The term cross-pollination is used for the opposite case, where pollen from ...

in a population facilitates the maintenance of gynodioecy by increasing the inbreeding costs for hermaphrodites. 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. 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 Inbreeding depression is the reduced biological fitness caused by loss of genetic diversity as a consequence of inbreeding, the breeding of individuals closely related genetically. This loss of genetic diversity results from small population siz ...

. 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.

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. 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. 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. 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.

Maize Maize (; ''Zea mays''), also known as corn in North American English, is a tall stout grass that produces cereal grain. It was domesticated by indigenous peoples in southern Mexico about 9,000 years ago from wild teosinte. Native American ...

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.

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. 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

when compared with woody lineages. Herbaceous growth form is also associated with a reduced pollen limitation 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. Gynodioecy is rare because some sexual systems are more evolutionarily liable to change in certain lineages in comparison with others. It has been estimated that gynodioecy occurs in 13.3% of ''

'' species.

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. 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 Inbreeding depression is the reduced biological fitness caused by loss of genetic diversity as a consequence of inbreeding, the breeding of individuals closely related genetically. This loss of genetic diversity results from small population siz ...

was found to be an important factor in the maintenance of gynodioecy in an endemic Hawaiian shrub ''

Schiedea adamantis ''Schiedea adamantis'', commonly known as Diamond Head schiedea, is a species of flowering plant in the family Caryophyllaceae, that is endemic to the island of Oahu in Hawaii. It inhabits low shrublands on steep slopes along the northwest rim o ...

'' occurring in a single population in Diamond Head Crater Oahu.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 Inbreeding depression, due to

selfing Autogamy or self-fertilization refers to the fusion of two gametes that come from one individual. Autogamy is predominantly observed in the form of self-pollination, a reproductive mechanism employed by many flowering plants. However, species of ...

in the

hermaphrodite A hermaphrodite () is a sexually reproducing organism that produces both male and female gametes. Animal species in which individuals are either male or female are gonochoric, which is the opposite of hermaphroditic. The individuals of many ...

s, was considered to be caused by the presence of many

mutation In biology, a mutation is an alteration in the nucleic acid sequence of the genome of an organism, virus, or extrachromosomal DNA. Viral genomes contain either DNA or RNA. Mutations result from errors during DNA or viral replication, ...

s of small effect.

Examples

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

Fuchsia excorticata ''Fuchsia excorticata'', commonly known as tree fuchsia, New Zealand fuchsia and by its Māori name , is a New Zealand native tree belonging to the family Onagraceae. It is commonly found throughout New Zealand and as far south as the Auckland ...

’’ * ''

'' * ''

'' *

* ''

Fragaria virginiana ''Fragaria virginiana'', known as Virginia strawberry, wild strawberry, common strawberry, or mountain strawberry, is a North American strawberry that grows across much of the United States and southern Canada. It is one of the two species of wi ...

'' * ''

Cucurbita foetidissima is a genus of herbaceous fruits in the gourd family, Cucurbitaceae (also known as ''cucurbits'' or ''cucurbi''), native to the Andes and Mesoamerica. Five edible species are grown and consumed for their flesh and seeds. They are variously ...

'' *

Wild thyme ''Thymus serpyllum'', known by the common names of Breckland thyme, Breckland wild thyme, wild thyme, creeping thyme, or elfin thyme, is a species of flowering plant in the mint family, Lamiaceae. It is a low, usually prostrate subshrub formin ...

* '' Daphne jezoensis'' * ''

Silene vulgaris ''Silene vulgaris'', the bladder campion or maidenstears, is a plant species of the genus ''Silene'' within the family ''Caryophyllaceae''. Native to the Old World, the plant has been naturalized elsewhere, including North America. The young sh ...

'' * ''

Silene nutans ''Silene nutans'' is a flowering plant in the genus ''Silene'', most commonly known as Nottingham catchfly. Description ''Silene nutans'' is a diploid, mainly outcrossing, herbaceous, perennial plant. It grows up to tall, from a branching, wood ...

'' * Plantains * ''

Reynoutria japonica ''Reynoutria japonica'', synonyms ''Fallopia japonica'' and ''Polygonum cuspidatum'', is a species of herbaceous perennial plant in the knotweed and buckwheat family Polygonaceae. Common names include Japanese knotweed and Asian knotweed. It is ...

'' *'' Erythranthe guttata''

References

{{reflist, 30em, refs= {{cite journal , vauthors = Delph LF, Touzet P, Bailey MF , title = Merging theory and mechanism in studies of gynodioecy , journal = Trends in Ecology & Evolution , volume = 22 , issue = 1 , pages = 17–24 , date = January 2007 , pmid = 17028054 , doi = 10.1016/j.tree.2006.09.013 , bibcode = 2007TEcoE..22...17D {{cite journal , vauthors = Preece T, Mao Y , title = The evolution of gynodioecy on a lattice , journal = Journal of Theoretical Biology , volume = 266 , issue = 2 , pages = 219–25 , date = September 2010 , pmid = 20599548 , doi = 10.1016/j.jtbi.2010.06.025 , bibcode = 2010JThBi.266..219P , s2cid = 8526610 , url = https://hal.archives-ouvertes.fr/hal-00614188/file/PEER_stage2_10.1016%252Fj.jtbi.2010.06.025.pdf {{Cite book , vauthors = Ridley M , title=The red queen: sex and the evolution of human nature , publisher=Penguin , year=1993 , pages=91–128 , isbn=978-0140167726 {{cite journal , vauthors = Rivkin LR, Case AL, Caruso CM , title = Why is gynodioecy a rare but widely distributed sexual system? Lessons from the Lamiaceae , journal = The New Phytologist , volume = 211 , issue = 2 , pages = 688–96 , date = July 2016 , pmid = 26991013 , doi = 10.1111/nph.13926 , doi-access = free , bibcode = 2016NewPh.211..688R {{cite journal , vauthors = Sinclair JP, Kameyama Y, Shibata A, Kudo G , title = Male-biased hermaphrodites in a gynodioecious shrub, Daphne jezoensis , journal = Plant Biology , volume = 18 , issue = 5 , pages = 859–67 , date = September 2016 , pmid = 27090773 , doi = 10.1111/plb.12463 , bibcode = 2016PlBio..18..859S {{Cite book , vauthors = Touzet P , veditors = Marechal-Drouard L , title=Mitochondrial genome evolution , year=2012 , chapter=Mitochondrial genome evolution and gynodioecy , series=Advances in botanical research , publisher=Academic Press , isbn=9780123944429 , pages=71–98 , chapter-url=https://books.google.com/books?id=YTmDrdXEAioC&q=pascal+touzet+advances+botanical+research {{cite journal , vauthors = Van de Paer C, Saumitou-Laprade P, Vernet P, Billiard S , title = The joint evolution and maintenance of self-incompatibility with gynodioecy or androdioecy , journal = Journal of Theoretical Biology , volume = 371 , pages = 90–101 , date = April 2015 , pmid = 25681148 , doi = 10.1016/j.jtbi.2015.02.003

Etymology

Evolution

Mechanism

Species distribution

Maintenance

Inbreeding depression

Examples

References

See also