Autogamy

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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 protists have also been observed using autogamy as a means of reproduction. Flowering plants engage in autogamy regularly, while the protists that engage in autogamy only do so in stressful environments.

Contents

Occurrence

Protists

Paramecium aurelia

Paramecium aurelia is the most commonly studied protozoan for autogamy. Similar to other unicellular organisms, Paramecium aurelia typically reproduce asexually via binary fission or sexually via cross-fertilization. However, studies have shown that when put under nutritional stress, Paramecium aurelia will undergo meiosis and subsequent fusion of gametic-like nuclei. [1] This process, defined as hemixis, a chromosomal rearrangement process, takes place in a number of steps. First, the two micronuclei of P. aurelia enlarge and divide two times to form eight nuclei. Some of these daughter nuclei will continue to divide to create potential future gametic nuclei. Of these potential gametic nuclei, one will divide two more times. Of the four daughter nuclei arising from this step, two of them become anlagen, or cells that will form part of the new organism. The other two daughter nuclei become the gametic micronuclei that will undergo autogamous self-fertilization. [2] These nuclear divisions are observed mainly when the P. aurelia is put under nutritional stress. Research shows that P. aurelia undergo autogamy synchronously with other individuals of the same species.

Clonal aging and rejuvenation

In Paramecium tetraurelia, vitality declines over the course of successive asexual cell divisions by binary fission. Clonal aging is associated with a dramatic increase in DNA damage. [3] [4] [5] When paramecia that have experienced clonal aging undergo meiosis, either during conjugation or automixis, the old macronucleus disintegrates and a new macronucleus is formed by replication of the micronuclear DNA that had just experienced meiosis followed by syngamy. These paramecia are rejuvenated in the sense of having a restored clonal lifespan. Thus it appears that clonal aging is due in large part to the progressive accumulation of DNA damage, and that rejuvenation is due to repair of DNA damage during meiosis that occurs in the micronucleus during conjugation or automixis and reestablishment of the macronucleus by replication of the newly repaired micronuclear DNA.

Tetrahymena rostrata

Similar to Paramecium aurelia, the parasitic ciliate Tetrahymena rostrata has also been shown to engage in meiosis, autogamy and development of new macronuclei when placed under nutritional stress. [6] Due to the degeneration and remodeling of genetic information that occurs in autogamy, genetic variability arises and possibly increases an offspring's chances of survival in stressful environments.

Allogromia laticollaris

Allogromia laticollaris is perhaps the best-studied foraminiferan amoeboid for autogamy. A. laticollaris can alternate between sexual reproduction via cross-fertilization and asexual reproduction via binary fission. The details of the life cycle of A. laticollaris are unknown, but similar to Paramecium aurelia, A. laticollaris is also shown to sometimes defer to autogamous behavior when placed in nutritional stress. As seen in Paramecium, there is some nuclear dimorphism observed in A. laticollaris. There are often observations of macronuclei and chromosomal fragments coexisting in A. laticollaris. This is indicative of nuclear and chromosomal degeneration, a process similar to the subdivisions observed in P. aurelia. Multiple generations of haploid A. laticollaris individuals can exist before autogamy actually takes place. [7] The autogamous behavior in A. laticollaris has the added consequence of giving rise to daughter cells that are substantially smaller than those rising from binary fission. [8] It is hypothesized that this is a survival mechanism employed when the cell is in stressful environments, and thus not able to allocate all resources to creating offspring. If a cell was under nutritional stress and not able to function regularly, there would be a strong possibility of its offspring's fitness being sub-par.

Self-pollination in flowering plants

About 10–15% of flowering plants are predominantly self-fertilizing. [9] Self-pollination is an example of autogamy that occurs in flowering plants. Self-pollination occurs when the sperm in the pollen from the stamen of a plant goes to the carpels of that same plant and fertilizes the egg cell present. Self-pollination can either be done completely autogamously or geitonogamously. In the former, the egg and sperm cells that unite come from the same flower. In the latter, the sperm and egg cells can come from a different flower on the same plant. While the latter method does blur the lines between autogamous self-fertilization and normal sexual reproduction, it is still considered autogamous self-fertilization. [10]

Self-pollination can lead to inbreeding depression due to expression of deleterious recessive mutations. [11] Meiosis followed by self-pollination results in little genetic variation, raising the question of how meiosis in self-pollinating plants is adaptively maintained over an extended period in preference to a less complicated and less costly asexual ameiotic process for producing progeny. For instance, Arabidopsis thaliana is a predominantly self-pollinating plant that has an outcrossing rate in the wild estimated at less than 0.3%, [12] and self-pollination appears to have evolved roughly a million years ago or more. [13] An adaptive benefit of meiosis that may explain its long-term maintenance in self-pollinating plants is efficient recombinational repair of DNA damage. [14]

Fungi

There are basically two distinct types of sexual reproduction among fungi. The first is outcrossing (in heterothallic fungi). In this case, mating occurs between two different haploid individuals to form a diploid zygote, that can then undergo meiosis. The second type is self-fertilization or selfing (in homothallic fungi). In this case, two haploid nuclei derived from the same individual fuse to form a zygote than can then undergo meiosis. Examples of homothallic fungi that undergo selfing include species with an aspergillus-like asexual stage (anamorphs) occurring in many different genera, [15] several species of the ascomycete genus Cochliobolus , [16] and the ascomycete Pneumocystis jirovecii [17] (for other examples, see Homothallism). A review of evidence on the evolution of sexual reproduction in the fungi led to the concept that the original mode of sexual reproduction in the last eukaryotic common ancestor was homothallic or self-fertile unisexual reproduction. [18]

Advantages

There are several advantages for the self-fertilization observed in flowering plants and protists. In flowering plants, it is important for some plants not to be dependent on pollinating agents that other plants rely on for fertilization. This is unusual, however, considering that many plant species have evolved to become incompatible with their own gametes. While these species would not be well served by having autogamous self-fertilization as a reproductive mechanism, other species, which do not have self-incompatibility, would benefit from autogamy. Protists have the advantage of diversifying their modes of reproduction. This is useful for a multitude of reasons. First, if there is an unfavorable change in the environment that puts the ability to deliver offspring at risk, then it is advantageous for an organism to have autogamy at its disposal. In other organisms, it is seen that genetic diversity arising from sexual reproduction is maintained by changes in the environment that favor certain genotypes over others. Aside from extreme circumstances, it is possible that this form of reproduction gives rise to a genotype in the offspring that will increase fitness in the environment. This is due to the nature of the genetic degeneration and remodeling intrinsic to autogamy in unicellular organisms. Thus, autogamous behavior may become advantageous to have if an individual wanted to ensure offspring viability and survival. This advantage also applies to flowering plants. However, it is important to note that this change has not shown to produce a progeny with more fitness in unicellular organisms. [19] It is possible that the nutrition deprived state of the parent cells before autogamy created a barrier for producing offspring that could thrive in those same stressful environments.

Disadvantages

In flowering plants, autogamy has the disadvantage of producing low genetic diversity in the species that use it as the predominant mode of reproduction. This leaves those species particularly susceptible to pathogens and viruses that can harm it. In addition, the foraminiferans that use autogamy have shown to produce substantially smaller progeny as a result. [20] This indicates that since it is generally an emergency survival mechanism for unicellular species, the mechanism does not have the nutritional resources that would be provided by the organism if it were undergoing binary fission.

Genetic consequences

Self-fertilization results in the loss of genetic variation within an individual (offspring), because many of the genetic loci that were heterozygous become homozygous. This can result in the expression of harmful recessive alleles, which can have serious consequences for the individual. The effects are most extreme when self-fertilization occurs in organisms that are usually out-crossing. [21] In plants, selfing can occur as autogamous or geitonogamous pollinations and can have varying fitness affects that show up as autogamy depression. After several generations, inbreeding depression is likely to purge the deleterious alleles from the population because the individuals carrying them have mostly died or failed to reproduce.

If no other effects interfere, the proportion of heterozygous loci is halved in each successive generation, as shown in the following table.

Illustration model of the decrease in genetic variation in a population of self-fertilized organisms derived from a heterozygous individual, assuming equal fitness

Generation AA
(%)		Aa
(%)		aa
(%)
P – 100 –
F1255025
F237.52537.5
F343.7512.543.75
F446.8756.2546.875
F548.43753.12548.4375
F649.218751.562549.21875
F749.6093750.7812549.609375
F849.80468750.39062549.8046875
F949.902343750.195312549.90234375
F1049.995117187 ≈ 50.0 0.09765626 ≈ 0.0 49.995117187 ≈ 50.0

Evolution

The evolutionary shift from outcrossing to self-fertilization is one of the most frequent evolutionary transitions in plants. Since autogamy in flowering plants and autogamy in unicellular species is fundamentally different, and plants and protists are not related, it is likely that both instances evolved separately. However, due to the little overall genetic variation that arises in progeny, it is not fully understood how autogamy has been maintained in the tree of life.

See also

Related Research Articles

<span class="mw-page-title-main">Asexual reproduction</span> Reproduction without a sexual process

Asexual reproduction is a type of reproduction that does not involve the fusion of gametes or change in the number of chromosomes. The offspring that arise by asexual reproduction from either unicellular or multicellular organisms inherit the full set of genes of their single parent and thus the newly created individual is genetically and physically similar to the parent or an exact clone of the parent. Asexual reproduction is the primary form of reproduction for single-celled organisms such as archaea and bacteria. Many eukaryotic organisms including plants, animals, and fungi can also reproduce asexually. In vertebrates, the most common form of asexual reproduction is parthenogenesis, which is typically used as an alternative to sexual reproduction in times when reproductive opportunities are limited. Komodo dragons and some monitor lizards can reproduce asexually.

<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">Reproduction</span> Biological process by which new organisms are generated from one or more parent organisms

Reproduction is the biological process by which new individual organisms – "offspring" – are produced from their "parent" or parents. There are two forms of reproduction: asexual and sexual.

<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, such as most flowering plants, that produces both types of gamete is a hermaphrodite.

<span class="mw-page-title-main">Fertilisation</span> Union of gametes of opposite sexes during the process of sexual reproduction to form a zygote

Fertilisation or fertilization, also known as generative fertilisation, syngamy and impregnation, is the fusion of gametes to give rise to a new individual organism or offspring and initiate its development. While processes such as insemination or pollination, which happen before the fusion of gametes, are also sometimes informally referred to as fertilisation, these are technically separate processes. The cycle of fertilisation and development of new individuals is called sexual reproduction. During double fertilisation in angiosperms, the haploid male gamete combines with two haploid polar nuclei to form a triploid primary endosperm nucleus by the process of vegetative fertilisation.

<i>Paramecium</i> Genus of unicellular ciliates, commonly studied as a representative of the ciliate group

Paramecium is a genus of eukaryotic, unicellular ciliates, commonly studied as a model organism of the ciliate group. Paramecium are widespread in freshwater, brackish, and marine environments and are often abundant in stagnant basins and ponds. Because some species are readily cultivated and easily induced to conjugate and divide, they have been widely used in classrooms and laboratories to study biological processes. The usefulness of Paramecium as a model organism has caused one ciliate researcher to characterize it as the "white rat" of the phylum Ciliophora.

<span class="mw-page-title-main">Biological life cycle</span> Series of stages of an organism

In biology, a biological life cycle is a series of stages of the life of an organism, that begins as a zygote, often in an egg, and concludes as an adult that reproduces, producing an offspring in the form of a new zygote which then itself goes through the same series of stages, the process repeating in a cyclic fashion.

<span class="mw-page-title-main">Mating</span> Process of pairing in biology

In biology, mating is the pairing of either opposite-sex or hermaphroditic organisms for the purposes of sexual reproduction. Fertilization is the fusion of two gametes. Copulation is the union of the sex organs of two sexually reproducing animals for insemination and subsequent internal fertilization. Mating may also lead to external fertilization, as seen in amphibians, fishes and plants. For most species, mating is between two individuals of opposite sexes. However, for some hermaphroditic species, copulation is not required because the parent organism is capable of self-fertilization (autogamy); for example, banana slugs.

<span class="mw-page-title-main">Self-pollination</span> Form of pollination

Self-pollination is a form of pollination in which pollen from the same plant arrives at the stigma of a flower or at the ovule. There are two types of self-pollination: in autogamy, pollen is transferred to the stigma of the same flower; in geitonogamy, pollen is transferred from the anther of one flower to the stigma of another flower on the same flowering plant, or from microsporangium to ovule within a single (monoecious) gymnosperm. Some plants have mechanisms that ensure autogamy, such as flowers that do not open (cleistogamy), or stamens that move to come into contact with the stigma. The term selfing that is often used as a synonym, is not limited to self-pollination, but also applies to other type of self-fertilization.

<span class="mw-page-title-main">Evolution of sexual reproduction</span> How sexually reproducing multicellular organisms could have evolved from a common ancestor species

Sexual reproduction is an adaptive feature which is common to almost all multicellular organisms and various unicellular organisms. Currently, the adaptive advantage of sexual reproduction is widely regarded as a major unsolved problem in biology. As discussed below, one prominent theory is that sex evolved as an efficient mechanism for producing variation, and this had the advantage of enabling organisms to adapt to changing environments. Another prominent theory, also discussed below, is that a primary advantage of outcrossing sex is the masking of the expression of deleterious mutations. Additional theories concerning the adaptive advantage of sex are also discussed below. Sex does, however, come with a cost. In reproducing asexually, no time nor energy needs to be expended in choosing a mate and, if the environment has not changed, then there may be little reason for variation, as the organism may already be well-adapted. However, very few environments have not changed over the millions of years that reproduction has existed. Hence it is easy to imagine that being able to adapt to changing environment imparts a benefit. Sex also halves the amount of offspring a given population is able to produce. Sex, however, has evolved as the most prolific means of species branching into the tree of life. Diversification into the phylogenetic tree happens much more rapidly via sexual reproduction than it does by way of asexual reproduction.

Heterothallic species have sexes that reside in different individuals. The term is applied particularly to distinguish heterothallic fungi, which require two compatible partners to produce sexual spores, from homothallic ones, which are capable of sexual reproduction from a single organism.

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.

<span class="mw-page-title-main">Mating in fungi</span> Combination of genetic material between compatible mating types

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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.

<i>Paramecium caudatum</i> Species of single-celled organism

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Homothallic refers to the possession, within a single organism, of the resources to reproduce sexually; i.e., having male and female reproductive structures on the same thallus. The opposite sexual functions are performed by different cells of a single mycelium.

<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.

<span class="mw-page-title-main">Ciliate</span> Taxon of protozoans with hair-like organelles called cilia

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Reproductive assurance occurs as plants have mechanisms to assure full seed set through selfing when outcross pollen is limiting. It is assumed that self-pollination is beneficial, in spite of potential fitness costs, when there is insufficient pollinator services or outcross pollen from other individuals to accomplish full seed set.. This phenomenon has been observed since the 19th century, when Darwin observed that self-pollination was common in some plants. Constant pollen limitation may cause the evolution of automatic selfing, also known as autogamy. This occurs in plants such as weeds, and is a form of reproductive assurance. As plants pursue reproductive assurance through self-fertilization, there is an increase in homozygosity, and inbreeding depression, due to genetic load, which results in reduced fitness of selfed offspring. Solely outcrossing plants may not be successful colonizers of new regions due to lack of other plants to outcross with, so colonizing species are expected to have mechanisms of reproductive assurance - an idea first proposed by Herbert G. Baker and referred to as Baker's "law" or "rule". Baker's law predicts that reproductive assurance affects establishment of plants in many contexts, including spread by weedy plants and following long-distance dispersal, such as occurs during island colonization. As plants evolve towards increase self-fertilization, energy is redirected to seed production rather than characteristics that increased outcrossing, such as floral attractants, which is a condition known as the selfing syndrome.

References

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