Environmental sex determination

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The sex of the green spoonworm, Bonellia viridis, a marine annelid, depends on where the larvae make landfall (female shown). Bonelie (Bonellia viridis) PC301461.JPG
The sex of the green spoonworm, Bonellia viridis , a marine annelid, depends on where the larvae make landfall (female shown).

Environmental sex determination is the establishment of sex by a non-genetic cue, such as nutrient availability, experienced within a discrete period after fertilization. [1] Environmental factors which often influence sex determination during development or sexual maturation include light intensity and photoperiod, temperature, nutrient availability, and pheromones emitted by surrounding plants or animals. This is in contrast to genotypic sex determination, which establishes sex at fertilization by genetic factors such as sex chromosomes. Under true environmental sex determination, once sex is determined, it is fixed and cannot be switched again. Environmental sex determination is different from some forms of sequential hermaphroditism in which the sex is determined flexibly after fertilization throughout the organism’s life. [2]

Contents

Adaptive significance

Environmental sex determination is similar to certain forms[ vague ] of sexual selection in that there are oftentimes different and opposing selective pressures on males and females because of the costs of reproduction. Sexual selection is common throughout the tree of life (most known in birds); often resulting in sexual dimorphism, or size and appearance differences between sexes in the same species. [3] In environmental sex determination, selective pressures over evolutionary time have selected for flexibility in sex determination to optimize fitness in a heterogenous environment because of the different costs of sex in males and females. [4] Certain environmental conditions differentially affect each sex such that it would be beneficial to become one sex and not the other. [5] This is especially pertinent for sessile organisms that cannot move to a different environment. In plants, for example, female sexual function is often more energetically expensive because once fertilized they must use significant stored energy to produce fruits, seeds, or sporophytes whereas males must only produce sperm (and sperm-containing structure; antheridium in seedless plants, and pollen in seed plants).

Mechanisms

Lacking genetic information coding for separate sexes such as sex chromosomes, individuals that exhibit environmental sex determination contain genetic information coding for both sexes on autosomes. [6] In general, once exposed to certain environmental cues, epigenetic changes cause developing individuals to become either male or female. Environmental cues that often trigger the development of males or females include temperature, nutrient (or food in the case of animals) and water availability, photoperiod, competitive stress, and pheromones from conspecific individuals. [7] [8] Specific mechanisms and cues vary between species.

Taxonomic range

Crustaceans

The amphipod crustacean Gammarus duebeni produces males early in the mating season, and females later, in response to the length of daylight, the photoperiod. Because male fitness improves more than female fitness with increased size, environmental sex determination is adaptive in this system by permitting males to experience a longer growing season than females. [9]

The branchiopod crustacean Daphnia magna parthenogenetically produces male progeny in response to a combination of three environmental factors, namely a reduced photoperiod in autumn, shortage of food and raised population density. [10]

Annelids

Bonellia viridis , a marine worm, has location-dependent sex determination; sex depends on where the larvae land. [11]

Vertebrates

The sex of alligators is determined by nest temperature. Crocnest.JPG
The sex of alligators is determined by nest temperature.

The sex of most amniote vertebrates, such as mammals and birds, is determined genetically. [12] However, some reptiles have temperature-dependent sex determination, where sex is permanently determined by thermal conditions experienced during the middle third of embryonic development. [13] [14] The sex of crocodilians and sphenodontians is exclusively determined by temperature. In contrast, squamates (lizards and snakes) and turtles exhibit both genotypic sex determination and temperature-dependent sex determination, although temperature dependence is much more common in turtles than in squamates. [15]

Ferns

A developing fern gametophyte. While in this immature, asexual stage, a fern gametophyte may undergo environmental sex determination based on cues from the surrounding environment. Fern young gametophyte.jpg
A developing fern gametophyte. While in this immature, asexual stage, a fern gametophyte may undergo environmental sex determination based on cues from the surrounding environment.

Most fern species (with a few exceptions, namely the Salvineales) are homosporous and lack sex chromosomes. Lacking genetic information coding for separate sexes, every fern spore has the capacity to become a male, female, or hermaphroditic gametophyte depending on the environment. [16] [17] In many fern species, including Ceratopteris richardii , environmental sex determination is linked to breeding systems. [18] Fern gametophytes exhibit a wide variety of breed systems which can be divided into outcrossing and inbreeding. To promote outcrossing, female gametophytes release a chemical pheromone known as Antheridiogen which controls the sex of nearby developing gametophytes. [19] Antheridiogen secreted by females promotes the development of nearby asexual gametophytes into males. This is adaptive because inducing maleness increases the probability of outcrossing as males provide sperm for the females rather than the females becoming hermaphroditic (or bisexual) and self-fertilizing. However, if no fertilization occurs, the female gametophyte can still become hermaphroditic and self-fertilize if the conditions are conducive to growth, ultimately resulting in inbreeding depression.

Additionally, similar to crocodilians, homosporous fern gametophyte sex is determined by the abiotic environment in accordance with the size-advantage model. In stressful environments (crowding or nutrient stress), gametophytes are smaller and develop into males. While in more favorable growing conditions, gametophytes are larger and develop into females. [20] [21]

Environmental sex determination in ferns based on nutrient availability, light, competition, and the pheromone Antheridiogen Environmental Sex Determination Fern gametophyte.jpg
Environmental sex determination in ferns based on nutrient availability, light, competition, and the pheromone Antheridiogen

Moss

Moss gametophytes (green photosynthetic tissue) and sporophytes (upright, brown structures). The presence of many sporophytes, indicates that the moss is likely either monoicous and self fertilizing or dioicous with fertile males and females. This can be rare as females often outcompete males in mosses. Moss 007.jpg
Moss gametophytes (green photosynthetic tissue) and sporophytes (upright, brown structures). The presence of many sporophytes, indicates that the moss is likely either monoicous and self fertilizing or dioicous with fertile males and females. This can be rare as females often outcompete males in mosses.

Moss gametophytes can be either asexual, female, male, or hermaphroditic like ferns. Unlike homosporous ferns, moss gametophytes can be either monoicous or dioicous (similar to monoecious and dioecious in vascular plants), with most studied dioicous species exhibiting genetic sex determination via the UV sex chromosome sex determination system. Some monoicous moss species such as Splachnum ampullaceum exhibit environmental sex determination during early development, with low light, low pH, and low nutrient availability all promoting male development. [22] In the presence of auxin, a widespread plant hormone, or gibberellins, compounds similar to Antheridiogen in ferns, both female and male individuals invest more in sexual structures (antheridia and archegonia). [23] Environmental sex determination in moss is fundamentally different from the spatial segregation of sexes, the occurrence of environmentally mediated sex ratios in moss patches, observed in sexually static moss species. Spatial segregation of the sexes in mosses is caused by differential survival rates between sexes as a result of the competitive advantage of female moss. [24] [25] This leads to female dominated populations maintained by asexual reproduction and minimal sexual reproduction. In contrast, environmental sex determination is the dynamic development of females or males in different environmental conditions.

Angiosperms

Flowering catasetum viridiflavum Catasetum viridiflavum.jpg
Flowering catasetum viridiflavum

Many angiosperms exhibit sequential hermaphroditism, meaning that they can switch sexes continually throughout their life based on the current conditions and resource availability to optimize fitness each flowering season. [26] But sequential hermaphroditism and environmental sex determination are not mutually exclusive. For example, Catasetum viridiflavum, an epiphyte (plant that grows on another plant) in the Orchidaceae family exhibits sequential hermaphroditism where the younger, smaller individuals have male inflorescences and the older, larger individuals have female inflorescences, but sex expression is also strongly influenced by light intensity. Individuals in high light are more often female and individuals in the low light are more often male, regardless of size. [27] [28] In higher light, individuals produce more ethylene, a common plant hormone, which promotes the formation of female flowers.

Related Research Articles

<span class="mw-page-title-main">Gamete</span> A haploid sex cell

A gamete 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. The name gamete was introduced by the German cytologist Eduard Strasburger.

<span class="mw-page-title-main">Gametophyte</span> Haploid stage in the life cycle of plants and algae

A gametophyte is one of the two alternating multicellular phases in the life cycles of plants and algae. It is a haploid multicellular organism that develops from a haploid spore that has one set of chromosomes. The gametophyte is the sexual phase in the life cycle of plants and algae. It develops sex organs that produce gametes, haploid sex cells that participate in fertilization to form a diploid zygote which has a double set of chromosomes. Cell division of the zygote results in a new diploid multicellular organism, the second stage in the life cycle known as the sporophyte. The sporophyte can produce haploid spores by meiosis that on germination produce a new generation of gametophytes.

<span class="mw-page-title-main">Sex</span> Trait that determines an organisms sexually reproductive function

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.

<span class="mw-page-title-main">Sex-determination system</span> Biological system that determines the development of an organisms sex

A sex-determination system is a biological system that determines the development of sexual characteristics in an organism. Most organisms that create their offspring using sexual reproduction have two common sexes and a few less common intersex variations.

<span class="mw-page-title-main">Sporophyte</span> Diploid multicellular stage in the life cycle of a plant or alga

A sporophyte is the diploid multicellular stage in the life cycle of a plant or alga which produces asexual spores. This stage alternates with a multicellular haploid gametophyte phase.

<span class="mw-page-title-main">Sexual differentiation</span> Embryonic development of sex differences

Sexual differentiation is the process of development of the sex differences between males and females from an undifferentiated zygote. Sex determination is often distinct from sex differentiation; sex determination is the designation for the development stage towards either male or female, while sex differentiation is the pathway towards the development of the phenotype.

<span class="mw-page-title-main">Plant reproductive morphology</span> Parts of plant enabling sexual reproduction

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

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.

<span class="mw-page-title-main">Sequential hermaphroditism</span> Sex change as part of the normal life cycle of a species

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.

Sex allocation is the allocation of resources to male versus female reproduction in sexual species. Sex allocation theory tries to explain why many species produce equal number of males and females.

Plant reproduction is the production of new offspring in plants, which can be accomplished by sexual or asexual reproduction. Sexual reproduction produces offspring by the fusion of gametes, resulting in offspring genetically different from either parent. Asexual reproduction produces new individuals without the fusion of gametes, resulting in clonal plants that are genetically identical to the parent plant and each other, unless mutations occur.

<span class="mw-page-title-main">Sex chromosome</span> Chromosome that differs from an ordinary autosome in form, size, and behavior

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.

<i>Ceratopteris</i> Genus of aquatic plants

Ceratopteris is the only genus among homosporous ferns that is exclusively aquatic. It is pan-tropical and classified in the Parkerioideae subfamily of the family Pteridaceae.

<span class="mw-page-title-main">Hermaphrodite</span> Sexually reproducing organism that produces both male and female gametes

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.

<span class="mw-page-title-main">Female</span> Sex of an organism that produces ova

An organism's sex is female if it produces the ovum, the type of gamete that fuses with the male gamete during sexual reproduction.

<span class="mw-page-title-main">Sexual reproduction</span> Biological process

Sexual reproduction is a type of reproduction that involves a complex life cycle in which a gamete with a single set of chromosomes combines with another gamete to produce a zygote that develops into an organism composed of cells with two sets of chromosomes (diploid). This is typical in animals, though the number of chromosome sets and how that number changes in sexual reproduction varies, especially among plants, fungi, and other eukaryotes.

<i>Ceratopteris richardii</i> Species of aquatic plant

Ceratopteris richardii is a fern species belonging to the genus Ceratopteris, one of only two genera of the subfamily Parkerioideae of the family Pteridaceae. It is one of several genera of ferns adapted to an aquatic existence. C. richardii was previously regarded as being part of the species Ceratopteris thalictroides.

Antheridiogens are a class of chemicals secreted by fern gametophytes that have "been shown to influence production of male gametangia and thus mating systems in a large number of terrestrial fern species". Antheridiogens are only observed in homosporous fern species, as all gametophytes are potentially bisexual.

<span class="mw-page-title-main">Simultaneous hermaphroditism</span> One of the two types of hermaphroditism

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 same breeding season.

References

  1. ↑ JANZEN, F. J.; PHILLIPS, P. C. (November 2006). "Exploring the evolution of environmental sex determination, especially in reptiles". Journal of Evolutionary Biology. 19 (6): 1775–1784. doi:10.1111/j.1420-9101.2006.01138.x. ISSN   1010-061X. PMID   17040374. S2CID   15485510.
  2. ↑ Warner, Robert R. (January 1975). "The Adaptive Significance of Sequential Hermaphroditism in Animals". The American Naturalist. 109 (965): 61–82. doi:10.1086/282974. ISSN   0003-0147. S2CID   84279130.
  3. ↑ Parker, G.A. (1979), "Sexual Selection and Sexual Conflict", Sexual Selection and Reproductive Competition in Insects, Elsevier, pp. 123–166, doi:10.1016/b978-0-12-108750-0.50010-0, ISBN   978-0-12-108750-0 , retrieved 2020-11-17
  4. ↑ DeSoto, Lucía; Quintanilla, Luis G.; Méndez, Marcos (November 2008). "Environmental sex determination in ferns: effects of nutrient availability and individual density inWoodwardia radicans". Journal of Ecology. 96 (6): 1319–1327. doi: 10.1111/j.1365-2745.2008.01425.x . ISSN   0022-0477.
  5. ↑ McCabe, J.; Dunn, A. M. (1997). "Adaptive significance of environmental sex determination in an amphipod". Journal of Evolutionary Biology. 10 (4): 515. doi:10.1007/s000360050039. ISSN   1010-061X.
  6. ↑ Bull, J. J.; Vogt, R. C.; Bulmer, M. G. (March 1982). "Heritability of Sex Ratio in Turtles with Environmental Sex Determination". Evolution. 36 (2): 333–341. doi:10.2307/2408052. ISSN   0014-3820. JSTOR   2408052. PMID   28563174.
  7. ↑ Adams, Jonathan; Greenwood, Paul; Naylor, Caroline (March 1987). "Evolutionary Aspects of Environmental Sex Determination". International Journal of Invertebrate Reproduction and Development. 11 (2): 123–135. doi:10.1080/01688170.1987.10510273. ISSN   0168-8170.
  8. ↑ Dunn, Alison M.; Hogg, John C.; Kelly, Andrew; Hatcher, Melanie J. (January 2005). "Two cues for sex determination in Gammarus duebeni : Adaptive variation in environmental sex determination?". Limnology and Oceanography. 50 (1): 346–353. Bibcode:2005LimOc..50..346D. doi:10.4319/lo.2005.50.1.0346. ISSN   0024-3590.
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  10. ↑ Kato, Yasuhiko; Kobayashi, Kaoru; Watanabe, Hajime; Iguchi, Taisen (2011). "Environmental Sex Determination in the Branchiopod Crustacean Daphnia magna: Deep Conservation of a Doublesex Gene in the Sex-Determining Pathway". PLOS Genetics . 7 (3): 1–12. doi: 10.1371/journal.pgen.1001345 . PMC   3063754 . PMID   21455482.
  11. ↑ Gilbert, Scott (2006). Developmental biology (8th ed.). Sunderland, Mass.: Sinauer Associates. p.  552. ISBN   9780878932504.
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  14. ↑ Nicole Valenzuela; Valentine A. Lance, eds. (2004). Temperature Dependent Sex Determination in Vertebrates. Smithsonian Institution. ISBN   978-1-58834-203-4.
  15. ↑ Janzen, Fredric J.; Krenz, James G. (2004). "Phylogenetics: which was first, TSD or GSD?". In Nicole Valenzuela; Valentine A. Lance (eds.). Temperature Dependent Sex Determination in Vertebrates (PDF). Smithsonian Institution. pp. 121–130. ISBN   978-1-58834-203-4. Archived from the original (PDF) on 2015-09-24. Retrieved 2011-02-26.
  16. ↑ Goodnoe, Taylor T.; Hill, Jeffrey P.; Aho, Ken (April 2016). "Effects of variation in carbon, nitrogen, and phosphorus molarity and stoichiometry on sex determination in the fern Ceratopteris richardii". Botany. 94 (4): 249–259. doi:10.1139/cjb-2015-0187. ISSN   1916-2790.
  17. ↑ DeSoto, Lucía; Quintanilla, Luis G.; Méndez, Marcos (November 2008). "Environmental sex determination in ferns: effects of nutrient availability and individual density inWoodwardia radicans". Journal of Ecology. 96 (6): 1319–1327. doi: 10.1111/j.1365-2745.2008.01425.x . ISSN   0022-0477.
  18. ↑ Goodnoe, Taylor T.; Hill, Jeffrey P. (2018-05-20). "Plasticity of female reproductive resource allocation depends on the presence or absence of prior environmental sex determination inCeratopteris richardii". Ecology and Evolution. 8 (12): 6133–6143. doi: 10.1002/ece3.4159 . ISSN   2045-7758. PMC   6024121 . PMID   29988448.
  19. ↑ Chiou, Wen-Liang; Farrar, Donald R. (May 1997). "Antheridiogen production and response in Polypodiaceae species". American Journal of Botany. 84 (5): 633–640. doi: 10.2307/2445900 . ISSN   0002-9122. JSTOR   2445900. PMID   21708616.
  20. ↑ KORPELAINEN, HELENA (April 1994). "Growth, sex determination and reproduction of Dryopteris filix-mas (L.) Schott gametophytes under varying nutritional conditions". Botanical Journal of the Linnean Society. 114 (4): 357–366. doi:10.1111/j.1095-8339.1994.tb01840.x. ISSN   0024-4074.
  21. ↑ Pérez-Escobar, Oscar Alejandro; Chomicki, Guillaume; Condamine, Fabien L.; de Vos, Jurriaan M.; Martins, Aline C.; Smidt, Eric C.; Klitgård, Bente; Gerlach, Günter; Heinrichs, Jochen (2017-10-10). "Multiple Geographical Origins of Environmental Sex Determination enhanced the diversification of Darwin's Favourite Orchids". Scientific Reports. 7 (1): 12878. Bibcode:2017NatSR...712878P. doi: 10.1038/s41598-017-12300-y . ISSN   2045-2322. PMC   5635016 . PMID   29018291.
  22. ↑ Cameron, Randall G.; Wyatt, Robert (1990). "Spatial Patterns and Sex Ratios in Dioecious and Monoecious Mosses of the Genus Splachnum". The Bryologist. 93 (2): 161. doi:10.2307/3243620. ISSN   0007-2745. JSTOR   3243620.
  23. ↑ BHATLA, S. C.; CHOPRA, R. N. (1981). "Hormonal Regulation of Gametangial Formation in the MossBryum argenteumHedw". Journal of Experimental Botany. 32 (6): 1243–1256. doi:10.1093/jxb/32.6.1243. ISSN   0022-0957.
  24. ↑ Bowker, Matthew A.; Stark, Lloyd R.; McLetchie, D. Nicholas; Mishler, Brent D. (April 2000). "Sex expression, skewed sex ratios, and microhabitat distribution in the dioecious desert moss Syntrichia caninervis (Pottiaceae)". American Journal of Botany. 87 (4): 517–526. doi:10.2307/2656595. ISSN   0002-9122. JSTOR   2656595. PMID   10766723.
  25. ↑ Kobayashi, Kazuya; Hasegawa, Eisuke (April 2016). "A female-biased sex ratio reduces the twofold cost of sex". Scientific Reports. 6 (1): 23982. Bibcode:2016NatSR...623982K. doi: 10.1038/srep23982 . ISSN   2045-2322. PMC   4817508 . PMID   27035400.
  26. ↑ Policansky, D (November 1982). "Sex Change in Plants and Animals". Annual Review of Ecology and Systematics. 13 (1): 471–495. doi:10.1146/annurev.es.13.110182.002351. ISSN   0066-4162.
  27. ↑ Pérez-Escobar, Oscar Alejandro; Chomicki, Guillaume; Condamine, Fabien L.; de Vos, Jurriaan M.; Martins, Aline C.; Smidt, Eric C.; Klitgård, Bente; Gerlach, Günter; Heinrichs, Jochen (2017-10-10). "Multiple Geographical Origins of Environmental Sex Determination enhanced the diversification of Darwin's Favourite Orchids". Scientific Reports. 7 (1): 12878. Bibcode:2017NatSR...712878P. doi: 10.1038/s41598-017-12300-y . ISSN   2045-2322. PMC   5635016 . PMID   29018291.
  28. ↑ Zimmerman, Jess K. (April 1991). "Ecological Correlates of Labile Sex Expression in the Orchid Catasetum Viridiflavum". Ecology. 72 (2): 597–608. doi:10.2307/2937200. ISSN   0012-9658. JSTOR   2937200.
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