Maternal effect

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This article concerns the legitimate scientific concept of genes that are expressed only when carried by the female parent. It is not to be confused with the generally discredited theory of maternal impression.

A maternal effect is a situation where the phenotype of an organism is determined not only by the environment it experiences and its genotype, but also by the environment and genotype of its mother. In genetics, maternal effects occur when an organism shows the phenotype expected from the genotype of the mother, irrespective of its own genotype, often due to the mother supplying mRNA or proteins to the egg. Maternal effects can also be caused by the maternal environment independent of genotype, sometimes controlling the size, sex, or behaviour of the offspring. These adaptive maternal effects lead to phenotypes of offspring that increase their fitness. Further, it introduces the concept of phenotypic plasticity, an important evolutionary concept. It has been proposed that maternal effects are important for the evolution of adaptive responses to environmental heterogeneity.

Maternal effects in genetics[edit]

In genetics, a maternal effect occurs when the phenotype of an organism is determined by the genotype of its mother.[1] For example, if a mutation is maternal effect recessive, then a female homozygous for the mutation may appear phenotypically normal, however her offspring will show the mutant phenotype, even if they are heterozygous for the mutation.

Maternal effect
Maternal effect crosses1.svg
Maternal effect crosses2.svg
Maternal effect crosses3.svg
Maternal effect crosses4.svg
All offspring show the wild-type phenotype All offspring show the mutant phenotype
Genetic crosses involving a maternal effect recessive mutation, m. The maternal genotype determines the phenotype of the offspring.

Maternal effects often occur because the mother supplies a particular mRNA or protein to the oocyte, hence the maternal genome determines whether the molecule is functional. Maternal supply of mRNAs to the early embryo is important, as in many organisms the embryo is initially transcriptionally inactive.[2] Because of the inheritance pattern of maternal effect mutations, special genetic screens are required to identify them. These typically involve examining the phenotype of the organisms one generation later than in a conventional (zygotic) screen, as their mothers will be potentially homozygous for maternal effect mutations that arise.[3][4]

In Drosophila early embryogenesis[edit]

Protein and RNA are transported in particles (white dots) from the nurse cells (maternal) to the developing oocyte in Drosophila melanogaster. Scale bar shows 10µm.
For more details on the role of the maternal effect genes, see Drosophila embryogenesis.

A Drosophila melanogaster oocyte develops in an egg chamber in close association with a set of cells called nurse cells. Both the oocyte and the nurse cells are descended from a single germline stem cell, however cytokinesis is incomplete in these cell divisions, and the cytoplasm of the nurse cells and the oocyte is connected by structures known as ring canals.[5] Only the oocyte undergoes meiosis and contributes DNA to the next generation.

Many maternal effect Drosophila mutants have been found that affect the early steps in embryogenesis such as axis determination, including bicoid, dorsal, gurken and oskar.[6][7][8] For example, embryos from homozygous bicoid mothers fail to produce head and thorax structures.

Once the gene that is disrupted in the bicoid mutant was identified, it was shown that bicoid mRNA is transcribed in the nurse cells and then relocalized to the oocyte.[9] Other maternal effect mutants either affect products that are similarly produced in the nurse cells and act in the oocyte, or parts of the transportation machinery that are required for this relocalization.[10] Since these genes are expressed in the (maternal) nurse cells and not in the oocyte or fertilised embryo, the maternal genotype determines whether they can function.

In Birds[edit]

In birds, mothers may pass down hormones in their eggs that affect an offspring's growth and behavior. Experiments in domestic Canaries have shown that eggs that contain more yolk androgens develop into chicks that display more social dominance. Similar variation in yolk androgen levels have been seen in bird species like the American Coot, though the mechanism of effect has yet to be established.

Environmental maternal effects[edit]

The environment or condition of the mother can also in some situations influence the phenotype of her offspring, independent of the offspring's genotype.

Paternal effect genes[edit]

In contrast, a paternal effect is when a phenotype results from the genotype of the father, rather than the genotype of the individual.[11] The genes responsible for these effects are components of sperm that are involved in fertilization and early development.[12] An example of a paternal-effect gene is the ms(3)sneaky in Drosophila. Males with a mutant allele of this gene produce sperm that are able to fertilize an egg, but the sneaky-inseminated eggs do not develop normally. However, females with this mutation produce eggs that undergo normal development when fertilized.[13]

Adaptive Maternal Effects[edit]

Adaptive maternal effects induce phenotypic changes in offspring that result in an increase in fitness. These changes arise from mothers sensing environmental cues that work to reduce offspring fitness, and then responding to them in a way that then “prepares” offspring for their future environments. A key characteristic of “adaptive maternal effects” phenotypes, is their plasticity. Phenotypic plasticity gives organisms the ability to respond to different environments by altering their phenotype. With these “altered” phenotypes increasing fitness it becomes important to look at the likelihood that adaptive maternal effects will evolve and become a significant phenotypic adaptation to an environment.

Defining Adaptive Maternal Effects[edit]

When traits are influenced by either the maternal environment or the maternal phenotype, it is said to be influenced by maternal effects. Maternal effects work to alter the phenotypes of the offspring through pathways other than DNA.[14] Adaptive maternal effects are when these maternal influences lead to a phenotypic change that increases the fitness of the offspring. In general, adaptive maternal effects are a mechanism to cope with factors that work to reduce offspring fitness;[15] they are also environment specific.

It can sometimes be difficult to differentiate between maternal and adaptive maternal effects. Consider the following: Gypsy moths reared on foliage of black oak, rather than chestnut oak, had offspring that developed faster.[16] This is a maternal not an adaptive maternal effect. In order to be an adaptive maternal effect, the mother’s environment would have to have led to a change in the eating habits or behavior of the offspring.[16] The key difference between the two therefore, is that adaptive maternal effects are environment specific. The phenotypes that arise are in response to the mother sensing an environment that would reduce the fitness of her offspring. By accounting for this environment she is then able to alter the phenotypes to actually increase the offspring’s fitness. Maternal effects are not in response to an environmental cue, and further they have the potential to increase offspring fitness, but they may not.

When looking at the likelihood of these “altered” phenotypes evolving there are many factors and cues involved. Adaptive maternal effects evolve only when: offspring can face many potential environments; when a mother can “predict” the environment in which her offspring will be born into; and when a mother can influence her offspring’s phenotype, thereby increasing their fitness.[16] The summation of all of these factors can then lead to these “altered” traits becoming favorable for evolution.

The phenotypic changes that arise from adaptive maternal effects are a result of the mother sensing that a certain aspect of the environment may decrease the survival of her offspring. When sensing a cue the mother “relays” information to the developing offspring and therefore induces adaptive maternal effects. This tends to then cause the offspring to have a higher fitness because they are “prepared” for the environment they are likely to experience.[15] These cues can include responses to predators, habitat, high population density, and food availability[17][18][19]

The increase in size of Northern American Red Squirrels is a great example of an adaptive maternal effect producing a phenotype that resulted in an increased fitness. The adaptive maternal effect was induced by the mothers sensing the high population density and correlating it to low food availability per individual. Her offspring were on average larger than other squirrels of the same species; they also grew faster. Ultimately, the squirrels born during this period of high population density showed an increased survival rate (and therefore fitness) during their first winter.[17]

Phenotypic Plasticity[edit]

When analyzing the types of changes that can occur to a phenotype, we can see changes that are behavioral, morphological, or physiological. A characteristic of the phenotype that arises through adaptive maternal effects, is the plasticity of this phenotype. Phenotypic plasticity allows organisms to adjust their phenotype to various environments, thereby enhancing their fitness to changing environmental conditions.[15] Ultimately it is a key attribute to an organism’s, and a population’s, ability to adapt to short term environmental change.[20]

Phenotypic plasticity can be seen in many organisms, one species that exemplifies this concept is the seed beetle Stator limbatus. This seed beetle reproduces on different host plants, two of the more common ones being Cercidium floridum and Acacia greggii. When C. floridum is the host plant, there is selection for a large egg size; when A. greggii is the host plant, there is a selection for a smaller egg size. In an experiment it was seen that when a beetle who usually laid eggs on A. greggii was put onto C. floridum, the survivorship of the laid eggs was lower compared to those eggs produced by a beetle that was conditioned and remained on the C. florium host plant. Ultimately these experiments showed the plasticity of egg size production in the beetle, as well as the influence of the maternal environment on the survivorship of the offspring.[18]

See also[edit]

Other scientific topics that are related to adaptive maternal effects include epigenetics. Epigenetics is the study of changes in gene expression by methods other than direct changes to DNA. This “change” is often DNA methylation which is the addition of methyl groups to the DNA. When DNA is methylated, the gene that is located in the area in which this methylation has occurred, cannot be expressed. Inducing of DNA methylation is highly influenced by the maternal environment. Some maternal environments can lead to a higher methylation of an offspring’s DNA, while others a lower methylation.[21] The fact that methylation can be influenced by the maternal environment, makes it similar to adaptive maternal effects. Further similarities are seen by the fact that methylation can often increase the fitness of the offspring.

Further Examples of Adaptive Maternal Effects[edit]

In many insects:

  • Cues such as rapidly cooling temperatures or decreasing daylight can result in offspring that enter into a dormant state. They therefore will better survive the cooling temperatures and preserve energy.[22]
  • When forced to lay eggs on environments with low nutrients, offspring will be provided with more resources such higher nutrients through an increased egg size.[18]
  • Cues such as poor habitat or crowding can lead to offspring with wings. The wings allow the offspring to move away from poor environments to ones that will provide better resources.[22]


See also[edit]

References[edit]

  1. ^ Griffiths, Anthony J. F. (1999). An Introduction to genetic analysis. New York: W. H. Freeman. ISBN 0-7167-3771-X. 
  2. ^ Schier AF (April 2007). "The maternal-zygotic transition: death and birth of RNAs". Science 316 (5823): 406–7. Bibcode:2007Sci...316..406S. doi:10.1126/science.1140693. PMID 17446392. 
  3. ^ Jorgensen EM, Mango SE (May 2002). "The art and design of genetic screens: Caenorhabditis elegans". Nat. Rev. Genet. 3 (5): 356–69. doi:10.1038/nrg794. PMID 11988761. 
  4. ^ St Johnston D (March 2002). "The art and design of genetic screens: Drosophila melanogaster". Nat. Rev. Genet. 3 (3): 176–88. doi:10.1038/nrg751. PMID 11972155. 
  5. ^ Bastock R, St Johnston D (December 2008). "Drosophila oogenesis". Curr. Biol. 18 (23): R1082–7. doi:10.1016/j.cub.2008.09.011. PMID 19081037. 
  6. ^ Nüsslein-Volhard C, Lohs-Schardin M, Sander K, Cremer C (January 1980). "A dorso-ventral shift of embryonic primordia in a new maternal-effect mutant of Drosophila". Nature 283 (5746): 474–6. Bibcode:1980Natur.283..474N. doi:10.1038/283474a0. PMID 6766208. 
  7. ^ Schüpbach T, Wieschaus E (February 1986). "Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila". Dev. Biol. 113 (2): 443–8. doi:10.1016/0012-1606(86)90179-X. PMID 3081391. 
  8. ^ Nüsslein-Volhard C, Frohnhöfer HG, Lehmann R (December 1987). "Determination of anteroposterior polarity in Drosophila". Science 238 (4834): 1675–81. Bibcode:1987Sci...238.1675N. doi:10.1126/science.3686007. PMID 3686007. 
  9. ^ Berleth T, Burri M, Thoma G, et al. (June 1988). "The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo". EMBO J. 7 (6): 1749–56. PMC 457163. PMID 2901954. 
  10. ^ Ephrussi A, St Johnston D (January 2004). "Seeing is believing: the Bicoid morphogen gradient matures". Cell 116 (2): 143–52. doi:10.1016/S0092-8674(04)00037-6. PMID 14744427. 
  11. ^ Yasuda GK, Schubiger G, Wakimoto BT (1 May 1995). "Genetic characterization of ms (3) K81, a paternal effect gene of Drosophila melanogaster". Genetics 140 (1): 219–29. PMC 1206549. PMID 7635287. 
  12. ^ Fitch KR, Yasuda GK, Owens KN, Wakimoto BT (1998). "Paternal effects in Drosophila: implications for mechanisms of early development". Curr. Top. Dev. Biol. 38: 1–34. doi:10.1016/S0070-2153(08)60243-4. PMID 9399075. 
  13. ^ Fitch KR, Wakimoto BT (1998). "The paternal effect gene ms(3)sneaky is required for sperm activation and the initiation of embryogenesis in Drosophila melanogaster". Dev. Biol. 197 (2): 270–82. doi:10.1006/dbio.1997.8852. PMID 9630751. 
  14. ^ [1], Adkins-Regan, E.; Banerjee, S. B.; Correa, S. M.; Schweitzer, C. C. (2013). "Maternal effects in quail and zebra finches: Behavior and hormones". General and Comparative Endocrinology 190: 34. doi:10.1016/j.ygcen.2013.03.002.  edit
  15. ^ a b c [2], L. Galloway.Galloway, L. F. (2005). "Maternal effects provide phenotypic adaptation to local environmental conditions". New Phytologist 166: 93. doi:10.1111/j.1469-8137.2004.01314.x.  edit
  16. ^ a b c [3].
  17. ^ a b [4], density triggers maternal hormones. Dantzer, B.; Newman, A. E. M.; Boonstra, R.; Palme, R.; Boutin, S.; Humphries, M. M.; McAdam, A. G. (2013). "Density Triggers Maternal Hormones That Increase Adaptive Offspring Growth in a Wild Mammal". Science 340 (6137): 1215. doi:10.1126/science.1235765.  edit
  18. ^ a b c [5].
  19. ^ [6].
  20. ^ [7].Nussey, D. H.; Wilson, A. J.; Brommer, J. E. (2007). "The evolutionary ecology of individual phenotypic plasticity in wild populations". Journal of Evolutionary Biology 20 (3): 831. doi:10.1111/j.1420-9101.2007.01300.x.  edit
  21. ^ Survival of the Sickest (book).
  22. ^ a b [8]. Mousseau, T. A.; Fox, C. W. (1998). "The adaptive significance of maternal effects". Trends in ecology & evolution 13 (10): 403–7. PMID 21238360.  edit