The Quantitative Genetics Term Paper                                                    Gang Chen


Maternal Inheritance



     Inheritance is one of the most important themes that we have to address in genetics field. The inherited characters can be transported from sires to progenies via 2 kinds of vehicles: nucleus (chromosomes) and cytoplasm (mitochondrial DNA or chloroplast DNA). Inheritance through the chromosomes means that the chromatic substance of the nucleus is the locus of determiners, and since the substance of the nuclear content of egg and sperm is equivalent, this must also mean an equal determinative share by male and female in heredity. Inheritance through the cytoplasm means that the locus of the determiners or representatives of a character is the cytoplasm, and since it is the egg alone which contains any significant amount of cytoplasm, this inheritance usually is refer to as maternal inheritance (Dunn, 1917). Maternal inheritance has a great influence on the offspring’s gene action, fitness and evolution and it is involved in a wide variety of taxa.

     In contrast to nuclear inheritance, cytoplasmic inheritance in mammals is derived mostly, if not exclusively, from the maternal line. Mitochondria, and their DNA molecules (mtDNA), are the genetic units of this method of inheritance. Mitochondrial genes, in the contrast to genes in the nucleus, have an exclusively maternal mode of inheritance in mammals (Giles et al., 1980). Numerous mechanisms are responsible for maternal inheritance. The predominance of mitochondria of maternal origin in the offspring can be partially explained by the fact that at fertilization the spermatozoon contains approximately 75 mitochondria compare with approximately 100,000 mitochondria in the ooplasm in mice and cattle. Thus there is a 1:1000 ratio between paternal and maternal mtDNA molecules (Michaels et al., 1982; Gyllensten et al., 1985). Maternal inheritance of chloroplast DNA in higher plants is believed to be governed by methylation of specific DNA sites on maternal organelle, which protects it from degradation in the zygote (Sager and Grabowy, 1983). However, an extensive study in CD1 mice showed no difference in the state of methylation of mtDNA among oocytes, spermatozoa and earlier testicular cell types and between germinal and somatic cells of rats (Hecht et al., 1984). Therefore, it is believed that the maternal inheritance in mtDNA is not via the mechanism of gene methylatilon. Another example of interaction between cytoplasm and nucleus is the soy bean, Glycine hispida Maxim., which shows as different types two cotyledon colors, yellow and green. The beans with yellow cotyledons have two types of seed-coat colors, namely, green and yellow, while the beans with green cotyledons always have green seed-coats. The inheritance of these types of cotyledons and seed-coats has been proved to be maternal (Terao, 1918). Moreover, the early development of all metazoan embryos involves RNA transcripts and other cytoplasmic factors packaged in the egg by the mother during oogenesis. Embryogenesis, therefore, involves characters that are maternally inherited. Mitochondria, Chloroplasts, and other cytoplasmic factors that have physiological effects throughout the life of an individual are transmitted directly from one parent to the offspring, often through the mother (Kirkpatrick and Lande, 1989).

     Maternal inheritance is known from a wide variety of taxa. Body size in mammals, for example, typically shows effects from the uterine environment and maternal lactation performance (Bradford, 1972). In addition to mammals, maternal influences can be strong during the rearing of offspring. Bondari et al., (1978) carried out a study on insect, tribolium castaneum, and showed that genotypic values for rapid pupa growth are associated with the genotypic values for poor maternal effects. Reznick (1981) found that there was a greater than two-fold difference in offspring weight between populations of the mosquito fish Gambusia affinis, an ovoviviparous poeciliid. The genotype of  the mother, rather than the genotype of the offspring, determines offspring weight via two hybridization experiments. Price and Grant (1985) utilized a quantitative genetic analysis of growth from hatching in one species of Darwin's ground finch, Geospiza fortis, and revealed that:  (1) the presence of maternal effects influencing offspring size for the first few days after hatching; (2) high genetic correlations between adult and chick size from age day 3 onward; and (3) the presence of among-brood variance in shape from hatching onward. Additionally,large maternal effects have been found in many natural populations of animals. In collared flycatchers, over 25% of variation in clutch size was attributed to maternal effects (Schulter and Gustafsson 1993), and significant maternal effects have also been reported for a range of life-history traits in red deer including total fitness (Kruuk et al., 2002). The ability to quantify the genetic basis of maternal effects (i.e., indirect genetic effects) and the direct-indirect genetic covariance, however, has been limited to captive animals (Thiede 1998). In plants, controlled breeding designs under combined greenhouse and field conditions suggest that indirect genetic effects can either accelerate or constrain the potential response to selection (Thiede 1998).

         Evolution by natural selection pervades all aspects of biology, but an evolutionary response to selection can occur only if the trait under selection has a genetic basis. Most studies of natural populations have estimated only direct genetic effects (heritability), but some of theoretical and laboratory work suggests that heritable maternal effects can have important indirect influences on the potential for evolution (Wolf et al., 1998). Maternal effects arise when the phenotype of a mother or the environment she experiences has a phenotypic effect on her offspring. Dickerson expanded the simple definition of heritability (h2 = VAO/VPO), to include not just direct genetic effect (VAO), but also indirect genetic effects (VAM) and the direct-indirect genetic covariance (Cov[AO,AM]) as a proportion of the total phenotypic variation (VPO) in the offspring trait (Mcdam et al., 2002):

Ht2 = [VAO + 1/2VAM + 3/2 Cov (AO, AM)]/VPO.


     Experimental studies have shown that maternal inheritance can produce qualitatively different evolutionary outcomes than does simple Mendelian inheritance. Falconer (1965) found that artificial selection on litter size in mice results in a temporarily reversed evolutionary response. In the first generation of his experiment, selection on litter size produced offspring whose litters were smaller, while selection for decreased litter size produced offspring whose litters were large. Falconer inferred that this was the consequence of maternal effect acting through the body size of mothers. Another striking example of maternal inheritance is the strongly negative mother-offspring correlation for age at maturity in natural populations of the springtail Orchesella cincta (Janssen et al., 1988).


     As a result of such experimentation, animal breeders have long been interested in maternal inheritance because of its substantial effects on the results of artificial selection. This interest has led to models for the evolution of a single trait that maternally affects itself (Falconer, 1965), and for the evolution of two traits, one of which maternally affects the other (Van Vleck et al., 1977; Cheverud, 1984). The two-character model has been extended to cases in which the maternally affected trait is sexually dimorphic and in which the maternal character affects its own expression as well as that of the offspring character (Willham, 1972). Growth in body size, and particularly growth in body mass, was subject to large maternal effects, which accounted for more than 80% of the total phenotypic variation in growth in body mass. These large maternal effects were correlated with litter size and parturition date, which were themselves heritable. The combination of these two maternal traits resulted in a heritability of maternal performance, which is lower than most previous estimates of h2m from laboratory animals, but provides evidence for a potential indirect contribution of maternal performance to the evolution of offspring traits in a natural population of animals. The consideration of both direct and indirect genetic effects revealed a greater than three-fold increase in the potential for evolution of growth in body mass relative to that predicted by direct genetic effects alone (McAdam et al., 2002).


     In conclusion, maternal inheritance has a great influence on the offspring’s growth, gene action, fitness and evolution and it is involved in a wide variety of taxa. Though more research is needed to determine the clear mechanism involved in maternal inheritance and maternal selection, many biologists are interested in this field. It may be used as a useful tool to create ‘new’ breeds of livestock carrying the best of both nuclear and mitochondrial genes. The study will have important implication not only for our understanding of mitochondrial genetics and diseases in humans but for the increased productivity of animals and plants.




  1.  Bondari, K., Willham R. L., Freeman, A. E. 1978. Estimates of direct and maternal genetic correlations for pupa weight and family size of tribolum. J. Anim. Sci. 47:358-365.                             


  1. Bradford G. E. 1972. The role of maternal effects in animal breeding: VII. Maternal effects in sheep. J. Anim. Sci. 35:1324-1334.


  1. Cheverud, J. M. 1983. Evolution by kin selection: a quantitative genetic model illustrated by maternal performance in mice. Evolution. 38:766-777.


  1. Dunn, L. C. 1917. Nucleus and cytoplasm as vehicles of heredity. AM. Nat. 605:286-   300.


  1. Falconer, D. S. 1965. Maternal effects and selection response. P763-764 in S. J. Greet, ed. Genetics today: proceedings of the XI international congress of genetics. Vol. 3. Pergamon, Oxford.


  1. Giles RE, Blanc H, Cann HM, Wallace DC. 1980. Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci U S A. 77:6715-9.


  1. Gyllensten U, Wharton D, Wilson AC. 1985. Maternal inheritance of mitochondrial DNA during backcrossing of two species of mice. J Hered. 76:321-4.


  1. Hecht NB, Liem H, Kleene KC, Distel RJ, Ho SM. 1984. Maternal inheritance of the mouse mitochondrial genome is not mediated by a loss or gross alteration of the paternal mitochondrial DNA or by methylation of the oocyte mitochondrial DNA.
    Dev Biol. 102:452-61.


  1. Janssen, G. M., Jong, G., Joosse, E. N. G., Scharloo, W. 1988. A negative maternal effect in springtails. Evolution. 42:828-834.


  1. Kirkpatrick, M., Lande, R. 1989. The Evolution of Maternal Characters.  Evolution. 43: 485-503.


  1. Kruuk, L. E. B., Clutton-Brock, T. H., Slate, J., Pemberton, J. M., Brotherstone, S., Guinness, F. E. 2000. Heritability of fitness in a wild mammal population. Heredity. 97: 698-703.


  1. Michaels GS, Hauswirth WW, Laipis PJ. 1982. Mitochondrial DNA copy number in bovine oocytes and somatic cells. Dev Biol. 94:246-51.


  1. Price, T. D., Grant, P. R. 1985. The evolution of ontogeny in Darwin’s finches: a quantitative genetic approach. Am. Nat. 125:169-188.


  1. Reznick, D. 1981. "Grandfather Effects": The Genetics of Interpopulation Differences in Offspring Size in the Mosquito Fish. Evolution. 35:941-953.


  1. Sager R and Grabowy C. 1983. Differential methylarion of chloroplast DNA regulates maternal inheritance in a methylated mutant of chlamydomonas. Proceedings of the National Academy of sciences of USA. 80:3025-3029.


  1. Terao, H. 1918. Maternal inheritance in the soy bean. Am. Nat. 613:51-56.


  1. Van Vleck, L. D., Louis, D. S., Miller, J. I. 1977. Expected phynotypic response in weaning weight of beef calves from selection for direct and maternal genetic effects. J. Anim, Sci. 44:360-367.


  1. Wade, M. J. 2001. Maternal effect genes and the evolution of sociality in haplo-diploid organisms. Evolution. 55: 453-458.


  1. Willham, R. L. 1972. The role of maternal effects in animal breeding: III. Biometrical aspects of maternal effects in animals. J. Anim. Sci. 35:1288-1293.


  1. Thiede, D. A. 1998. Maternal inheritance and its effect on adaptive evolution: a quantitative genetic analysis of maternal effects in a natural plant population. evolution. 52:998-1015.


  1. Schluter, D., Gustafsson L. 1993. Species Recognition and Sexual Selection as a Unitary Problem in Animal Communication. Evolution. 48:658-667.


  1. McAdam, A. G., Boutin, S., Réale, D., Berteaux, D. 2002. Maternal effects and the   potential for evolution in a natural population of animals. Evolution. 56:846-851.


  1. Wolf, J. B. 2000. Gene interactions from maternal effects. Evolution. 54: 1882-1898.