Heterosis

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Time course imaging of two maize inbreds and their F1 hybrid (middle) exhibiting heterosis. Time course imaging of two maize inbreds LH198 and PHG47 and their F1 hybrid.gif
Time course imaging of two maize inbreds and their F1 hybrid (middle) exhibiting heterosis.

Heterosis, hybrid vigor, or outbreeding enhancement is the improved or increased function of any biological quality in a hybrid offspring. An offspring is heterotic if its traits are enhanced as a result of mixing the genetic contributions of its parents. The heterotic offspring often has traits that are more than the simple addition of the parents' traits, and can be explained by Mendelian or non-Mendelian inheritance. [1] Typical heterotic/hybrid traits of interest in agriculture are higher yield, quicker maturity, stability, drought tolerance [2] etc.

Contents

Definitions

In proposing the term heterosis to replace the older term heterozygosis, G.H. Shull aimed to avoid limiting the term to the effects that can be explained by heterozygosity in Mendelian inheritance. [3]

The physiological vigor of an organism as manifested in its rapidity of growth, its height and general robustness, is positively correlated with the degree of dissimilarity in the gametes by whose union the organism was formed … The more numerous the differences between the uniting gametes — at least within certain limits — the greater on the whole is the amount of stimulation … These differences need not be Mendelian in their inheritance … To avoid the implication that all the genotypic differences which stimulate cell-division, growth and other physiological activities of an organism are Mendelian in their inheritance and also to gain brevity of expression I suggest … that the word 'heterosis' be adopted.

Heterosis is often discussed as the opposite of inbreeding depression, although differences in these two concepts can be seen in evolutionary considerations such as the role of genetic variation or the effects of genetic drift in small populations on these concepts. Inbreeding depression occurs when related parents have children with traits that negatively influence their fitness largely due to homozygosity. In such instances, outcrossing should result in heterosis.

Not all outcrosses result in heterosis. For example, when a hybrid inherits traits from its parents that are not fully compatible, fitness can be reduced. This is a form of outbreeding depression, the effects of which are similar to inbreeding depression. [4]

Genetic and epigenetic bases

Since the early 1900s, two competing genetic hypotheses, not necessarily mutually exclusive, have been developed to explain hybrid vigor. More recently, an epigenetic component of hybrid vigor has also been established. [5] [6]

Dominance and overdominance

When a population is small or inbred, it tends to lose genetic diversity. Inbreeding depression is the loss of fitness due to loss of genetic diversity. Inbred strains tend to be homozygous for recessive alleles that are mildly harmful (or produce a trait that is undesirable from the standpoint of the breeder). Heterosis or hybrid vigor, on the other hand, is the tendency of outbred strains to exceed both inbred parents in fitness.

Selective breeding of plants and animals, including hybridization, began long before there was an understanding of underlying scientific principles. In the early 20th century, after Mendel's laws came to be understood and accepted, geneticists undertook to explain the superior vigor of many plant hybrids. Two competing hypotheses, which are not mutually exclusive, were developed: [7]

Genetic basis of heterosis. Dominance hypothesis. Scenario A. Fewer genes are under-expressed in the homozygous individual. Gene expression in the offspring is equal to the expression of the fittest parent. Overdominance hypothesis. Scenario B. Over-expression of certain genes in the heterozygous offspring. (The size of the circle depicts the expression level of gene A) Heterosis.svg
Genetic basis of heterosis. Dominance hypothesis. Scenario A. Fewer genes are under-expressed in the homozygous individual. Gene expression in the offspring is equal to the expression of the fittest parent. Overdominance hypothesis. Scenario B. Over-expression of certain genes in the heterozygous offspring. (The size of the circle depicts the expression level of gene A)

Dominance and overdominance have different consequences for the gene expression profile of the individuals. If overdominance is the main cause for the fitness advantages of heterosis, then there should be an over-expression of certain genes in the heterozygous offspring compared to the homozygous parents. On the other hand, if dominance is the cause, fewer genes should be under-expressed in the heterozygous offspring compared to the parents. Furthermore, for any given gene, the expression should be comparable to the one observed in the fitter of the two parents. In any case, outcross matings provide the benefit of masking deleterious recessive alleles in progeny. This benefit has been proposed to be a major factor in the maintenance of sexual reproduction among eukaryotes, as summarized in the article Evolution of sexual reproduction.

Historical retrospective

Which of the two mechanisms are the "main" reason for heterosis has been a scientific controversy in the field of genetics. [12] Population geneticist James Crow (1916–2012) believed, in his younger days, that overdominance was a major contributor to hybrid vigor. In 1998 he published a retrospective review of the developing science. [13] According to Crow, the demonstration of several cases of heterozygote advantage in Drosophila and other organisms first caused great enthusiasm for the overdominance theory among scientists studying plant hybridization. But overdominance implies that yields on an inbred strain should decrease as inbred strains are selected for the performance of their hybrid crosses, as the proportion of harmful recessives in the inbred population rises. Over the years, experimentation in plant genetics has proven that the reverse occurs, that yields increase in both the inbred strains and the hybrids, suggesting that dominance alone may be adequate to explain the superior yield of hybrids. Only a few conclusive cases of overdominance have been reported in all of genetics. Since the 1980s, as experimental evidence has mounted, the dominance theory has made a comeback.

Crow wrote:

The current view ... is that the dominance hypothesis is the major explanation of inbreeding decline and [of] the high yield of hybrids. There is little statistical evidence for contributions from overdominance and epistasis. But whether the best hybrids are getting an extra boost from overdominance or favorable epistatic contributions remains an open question. [13]

Epigenetics

An epigenetic contribution to heterosis has been established in plants, [6] and it has also been reported in animals. [14] MicroRNAs (miRNAs), discovered in 1993, are a class of non-coding small RNAs which repress the translation of messenger RNAs (mRNAs) or cause degradation of mRNAs. [15] In hybrid plants, most miRNAs have non-additive expression (it might be higher or lower than the levels in the parents). [6] This suggests that the small RNAs are involved in the growth, vigor and adaptation of hybrids. [6]

'Heterosis without hybridity' effects on plant size have been demonstrated in genetically isogenic F1 triploid (autopolyploid) plants, where paternal genome excess F1 triploids display positive heterosis, whereas maternal genome excess F1s display negative heterosis effects. [16] Such findings demonstrate that heterosis effects, with a genome dosage-dependent epigenetic basis, can be generated in F1 offspring that are genetically isogenic (i.e. harbour no heterozygosity). [16] [17] It has been shown [5] that hybrid vigor in an allopolyploid hybrid of two Arabidopsis species was due to epigenetic control in the upstream regions of two genes, which caused major downstream alteration in chlorophyll and starch accumulation. The mechanism involves acetylation or methylation of specific amino acids in histone H3, a protein closely associated with DNA, which can either activate or repress associated genes.

Specific mechanisms

Major histocompatibility complex in animals

One example of where particular genes may be important in vertebrate animals for heterosis is the major histocompatibility complex (MHC). Vertebrates inherit several copies of both MHC class I and MHC class II from each parent, which are used in antigen presentation as part of the adaptive immune system. Each different copy of the genes is able to bind and present a different set of potential peptides to T-lymphocytes. These genes are highly polymorphic throughout populations, but are more similar in smaller, more closely related populations. Breeding between more genetically distant individuals decreases the chance of inheriting two alleles that are the same or similar, allowing a more diverse range of peptides to be presented. This, therefore, increases the chance that any particular pathogen will be recognised, and means that more antigenic proteins on any pathogen are likely to be recognised, giving a greater range of T-cell activation, so a greater response. This also means that the immunity acquired to the pathogen is against a greater range of antigens, meaning that the pathogen must mutate more before immunity is lost. Thus, hybrids are less likely to succumb to pathogenic disease and are more capable of fighting off infection. This may be the cause, though, of autoimmune diseases.[ citation needed ]

Plants

Crosses between inbreds from different heterotic groups result in vigorous F1 hybrids with significantly more heterosis than F1 hybrids from inbreds within the same heterotic group or pattern. Heterotic groups are created by plant breeders to classify inbred lines, and can be progressively improved by reciprocal recurrent selection.

Heterosis is used to increase yields, uniformity, and vigor. Hybrid breeding methods are used in maize, sorghum, rice, sugar beet, onion, spinach, sunflowers, broccoli and to create a more psychoactive cannabis.

Corn (maize)

Nearly all field corn (maize) grown in most developed nations exhibits heterosis. Modern corn hybrids substantially outyield conventional cultivars and respond better to fertilizer.

Corn heterosis was famously demonstrated in the early 20th century by George H. Shull and Edward M. East after hybrid corn was invented by Dr. William James Beal of Michigan State University based on work begun in 1879 at the urging of Charles Darwin. Dr. Beal's work led to the first published account of a field experiment demonstrating hybrid vigor in corn, by Eugene Davenport and Perry Holden, 1881. These various pioneers of botany and related fields showed that crosses of inbred lines made from a Southern dent and a Northern flint, respectively, showed substantial heterosis and outyielded conventional cultivars of that era. However, at that time such hybrids could not be economically made on a large scale for use by farmers. Donald F. Jones at the Connecticut Agricultural Experiment Station, New Haven invented the first practical method of producing a high-yielding hybrid maize in 1914–1917. Jones' method produced a double-cross hybrid, which requires two crossing steps working from four distinct original inbred lines. Later work by corn breeders produced inbred lines with sufficient vigor for practical production of a commercial hybrid in a single step, the single-cross hybrids. Single-cross hybrids are made from just two original parent inbreds. They are generally more vigorous and also more uniform than the earlier double-cross hybrids. The process of creating these hybrids often involves detasseling.

Temperate maize hybrids are derived from two main heterotic groups: 'Iowa Stiff Stalk Synthetic', and nonstiff stalk.[ citation needed ]

Rice (Oryza sativa)

Hybrid rice sees cultivation in many countries, including China, India, Vietnam, and the Philippines. [18] Compared to inbred lines, hybrids produce approximately 20% greater yield, and comprise 45% of rice planting area in China. [19] Rice production has seen enormous rise in China due to heavy uses of hybrid rice. In China, efforts have generated a super hybrid rice strain ('LYP9') with a production capability around 15 tons per hectare. In India also, several varieties have shown high vigor, including 'RH-10' and 'Suruchi 5401'.[ citation needed ]

Since rice is a self-pollinating species, it requires the use of male-sterile lines to generate hybrids from separate lineages. The most common way of achieving this is using lines with genetic male-sterility, as manual emasculation is not optimal for large-scale hybridization. [20] The first generation of hybrid rice was developed in the 1970s. It relies on three lines: a cytoplasmic male sterile (CMS) line, a maintainer line, and a restorer line. [19] The second generation was widely adopted in the 1990s. [19] Instead of a CMS line, it uses an environment-sensitive genic male sterile line (EGMS), which can have its sterility reversed based on light or temperature. [20] This removes the need for a maintainer, making the hybridization and breeding process more efficient (albeit still high-maintenance). Second generation lines show a yield increase of 5-10% over first generation lines. [20] The third and current generation uses a nuclear male sterile line (NMS). Third generation lines have a recessive sterility gene, and their cultivation is more lenient towards maintainer lines and environmental conditions. Additionally, transgenes are only present in the maintainer, so hybrid plants can benefit from hybrid vigor without requiring special oversight. [19]

Animals

Hybrid livestock

The concept of heterosis is also applied in the production of commercial livestock. In cattle, crosses between Black Angus and Hereford produce a cross known as a "Black Baldy". In swine, "blue butts" are produced by the cross of Hampshire and Yorkshire. Other, more exotic hybrids (two different species, so genetically more dissimilar), such as "beefalo" which are hybrids of cattle and bison, are also used for specialty markets.

Poultry

Within poultry, sex-linked genes have been used to create hybrids in which males and females can be sorted at one day old by color. Specific genes used for this are genes for barring and wing feather growth. Crosses of this sort create what are sold as Black Sex-links, Red Sex-links, and various other crosses that are known by trade names.

Commercial broilers are produced by crossing different strains of White Rocks and White Cornish, the Cornish providing a large frame and the Rocks providing the fast rate of gain. The hybrid vigor produced allows the production of uniform birds at a marketable carcass weight at 6–9 weeks of age.

Likewise, hybrids between different strains of White Leghorn are used to produce laying flocks that provide the majority of white eggs for sale in the United States.

Dogs

In 2013, a study found that mixed breeds live on average 1.2 years longer than pure breeds. [21]

John Scott and John L. Fuller performed a detailed study of purebred Cocker Spaniels, purebred Basenjis, and hybrids between them. [22] They found that hybrids ran faster than either parent, perhaps due to heterosis. Other characteristics, such as basal heart rate, did not show any heterosis—the dog's basal heart rate was close to the average of its parents—perhaps due to the additive effects of multiple genes. [23]

Sometimes people working on a dog-breeding program find no useful heterosis. [24]

All this said, studies do not provide definitive proof of hybrid vigor in dogs. This is largely due to the unknown heritage of most mixed breed dogs used. Results vary wildly, with some studies showing benefit and others finding the mixed breed dogs to be more prone to genetic conditions. [25] [26] [27]

Birds

In 2014, a study undertaken by the Centre for Integrative Ecology at Deakin University in Geelong, Victoria, concluded that intraspecific hybrids between the subspecies Platycercus elegans flaveolus and P. e. elegans of the crimson rosella (P. elegans) were more likely to fight off diseases than their pure counterparts. [28]

Humans

Human beings are all extremely genetically similar to one another. [29] [30] [31] Michael Mingroni has proposed heterosis, in the form of hybrid vigor associated with historical reductions of the levels of inbreeding, as an explanation of the Flynn effect, the steady rise in IQ test scores around the world during the 20th century, [ citation needed ] though a review of nine studies found that there is no evidence to suggest inbreeding has an effect on IQ. [32]

Controversy

The term heterosis often causes confusion and even controversy, particularly in selective breeding of domestic animals, because it is sometimes (incorrectly) claimed that all crossbred plants and animals are "genetically superior" to their parents, due to heterosis,[ citation needed ]. but two problems exist with this claim:

  1. according to an article published in the journal Genome Biology , "genetic superiority" is an ill-defined term and not generally accepted terminology within the scientific field of genetics. [33] A related term fitness is well defined, but it can rarely be directly measured. Instead, scientists use objective, measurable quantities, such as the number of seeds a plant produces, the germination rate of a seed, or the percentage of organisms that survive to reproductive age. [34] From this perspective, crossbred plants and animals exhibiting heterosis may have "superior" traits, but this does not necessarily equate to any evidence of outright "genetic superiority". Use of the term "superiority" is commonplace for example in crop breeding, where it is well understood to mean a better-yielding, more robust plant for agriculture. Such a plant may yield better on a farm, but would likely struggle to survive in the wild, making this use open to misinterpretation. In human genetics any question of "genetic superiority" is even more problematic due to the historical and political implications of any such claim. Some may even go as far as to describe it as a questionable value judgement in the realm of politics, not science. [33]
  2. not all hybrids exhibit heterosis (see outbreeding depression).

An example of the ambiguous value judgements imposed on hybrids and hybrid vigor is the mule. While mules are almost always infertile, they are valued for a combination of hardiness and temperament that is different from either of their horse or donkey parents. While these qualities may make them "superior" for particular uses by humans, the infertility issue implies that these animals would most likely become extinct without the intervention of humans through animal husbandry, making them "inferior" in terms of natural selection.

See also

Related Research Articles

<span class="mw-page-title-main">Inbreeding</span> Reproduction by closely related organisms

Inbreeding is the production of offspring from the mating or breeding of individuals or organisms that are closely related genetically. By analogy, the term is used in human reproduction, but more commonly refers to the genetic disorders and other consequences that may arise from expression of deleterious recessive traits resulting from incestuous sexual relationships and consanguinity. Animals avoid inbreeding only rarely.

<span class="mw-page-title-main">Dominance (genetics)</span> One gene variant masking the effect of another in the other copy of the gene

In genetics, dominance is the phenomenon of one variant (allele) of a gene on a chromosome masking or overriding the effect of a different variant of the same gene on the other copy of the chromosome. The first variant is termed dominant and the second is called recessive. This state of having two different variants of the same gene on each chromosome is originally caused by a mutation in one of the genes, either new or inherited. The terms autosomal dominant or autosomal recessive are used to describe gene variants on non-sex chromosomes (autosomes) and their associated traits, while those on sex chromosomes (allosomes) are termed X-linked dominant, X-linked recessive or Y-linked; these have an inheritance and presentation pattern that depends on the sex of both the parent and the child. Since there is only one copy of the Y chromosome, Y-linked traits cannot be dominant or recessive. Additionally, there are other forms of dominance, such as incomplete dominance, in which a gene variant has a partial effect compared to when it is present on both chromosomes, and co-dominance, in which different variants on each chromosome both show their associated traits.

Inbred strains are individuals of a particular species which are nearly identical to each other in genotype due to long inbreeding. A strain is inbred when it has undergone at least 20 generations of brother x sister or offspring x parent mating, at which point at least 98.6% of the loci in an individual of the strain will be homozygous, and each individual can be treated effectively as clones. Some inbred strains have been bred for over 150 generations, leaving individuals in the population to be isogenic in nature. Inbred strains of animals are frequently used in laboratories for experiments where for the reproducibility of conclusions all the test animals should be as similar as possible. However, for some experiments, genetic diversity in the test population may be desired. Thus outbred strains of most laboratory animals are also available, where an outbred strain is a strain of an organism that is effectively wildtype in nature, where there is as little inbreeding as possible.

A heterozygote advantage describes the case in which the heterozygous genotype has a higher relative fitness than either the homozygous dominant or homozygous recessive genotype. Loci exhibiting heterozygote advantage are a small minority of loci. The specific case of heterozygote advantage due to a single locus is known as overdominance. Overdominance is a rare condition in genetics where the phenotype of the heterozygote lies outside of the phenotypical range of both homozygote parents, and heterozygous individuals have a higher fitness than homozygous individuals.

<span class="mw-page-title-main">Overdominance</span>

Overdominance is a phenomenon in genetics where the phenotype of the heterozygote lies outside the phenotypical range of both homozygous parents. Overdominance can also be described as heterozygote advantage regulated by a single genomic locus, wherein heterozygous individuals have a higher fitness than homozygous individuals. However, not all cases of the heterozygote advantage are considered overdominance, as they may be regulated by multiple genomic regions. Overdominance has been hypothesized as an underlying cause for heterosis.

F1 hybrid (also known as filial 1 hybrid) is the first filial generation of offspring of distinctly different parental types. F1 hybrids are used in genetics, and in selective breeding, where the term F1 crossbreed may be used. The term is sometimes written with a subscript, as F1 hybrid. Subsequent generations are called F2, F3, etc.

<span class="mw-page-title-main">Non-Mendelian inheritance</span> Type of pattern of inheritance

Non-Mendelian inheritance is any pattern in which traits do not segregate in accordance with Mendel's laws. These laws describe the inheritance of traits linked to single genes on chromosomes in the nucleus. In Mendelian inheritance, each parent contributes one of two possible alleles for a trait. If the genotypes of both parents in a genetic cross are known, Mendel's laws can be used to determine the distribution of phenotypes expected for the population of offspring. There are several situations in which the proportions of phenotypes observed in the progeny do not match the predicted values.

Genetics, a discipline of biology, is the science of heredity and variation in living organisms.

Genetic load is the difference between the fitness of an average genotype in a population and the fitness of some reference genotype, which may be either the best present in a population, or may be the theoretically optimal genotype. The average individual taken from a population with a low genetic load will generally, when grown in the same conditions, have more surviving offspring than the average individual from a population with a high genetic load. Genetic load can also be seen as reduced fitness at the population level compared to what the population would have if all individuals had the reference high-fitness genotype. High genetic load may put a population in danger of extinction.

<span class="mw-page-title-main">Molecular ecology</span> Subdiscipline of ecology

Molecular ecology is a subdiscipline of ecology that is concerned with applying molecular genetic techniques to ecological questions. It is virtually synonymous with the field of "Ecological Genetics" as pioneered by Theodosius Dobzhansky, E. B. Ford, Godfrey M. Hewitt, and others. These fields are united in their attempt to study genetic-based questions "out in the field" as opposed to the laboratory. Molecular ecology is related to the fields of population genetics and conservation genetics.

Complementation refers to a genetic process when two strains of an organism with different homozygous recessive mutations that produce the same mutant phenotype have offspring that express the wild-type phenotype when mated or crossed. Complementation will ordinarily occur if the mutations are in different genes. Complementation may also occur if the two mutations are at different sites within the same gene, but this effect is usually weaker than that of intergenic complementation. When the mutations are in different genes, each strain's genome supplies the wild-type allele to "complement" the mutated allele of the other strain's genome. Since the mutations are recessive, the offspring will display the wild-type phenotype. A complementation test can test whether the mutations in two strains are in different genes. Complementation is usually weaker or absent if the mutations are in the same gene. The convenience and essence of this test is that the mutations that produce a phenotype can be assigned to different genes without the exact knowledge of what the gene product is doing on a molecular level. American geneticist Edward B. Lewis developed the complementation test.

Inbreeding depression is the reduced biological fitness that has the potential to result from inbreeding. The loss of genetic diversity that is seen due to inbreeding, results from small population size. Biological fitness refers to an organism's ability to survive and perpetuate its genetic material. Inbreeding depression is often the result of a population bottleneck. In general, the higher the genetic variation or gene pool within a breeding population, the less likely it is to suffer from inbreeding depression, though inbreeding and outbreeding depression can simultaneously occur.

In biology, outbreeding depression happens when crosses between two genetically distant groups or populations result in a reduction of fitness. The concept is in contrast to inbreeding depression, although the two effects can occur simultaneously. Outbreeding depression is a risk that sometimes limits the potential for genetic rescue or augmentations. It is considered postzygotic response because outbreeding depression is noted usually in the performance of the progeny.

Out-crossing or out-breeding is the technique of crossing between different breeds. This is the practice of introducing distantly related genetic material into a breeding line, thereby increasing genetic diversity.

<span class="mw-page-title-main">Edward Murray East</span> American geneticist

Edward Murray East was an American plant geneticist, botanist, agronomist and eugenicist. He is known for his experiments that led to the development of hybrid corn and his support of 'forced' elimination of the 'unfit' based on eugenic findings. He worked at the Bussey Institute of Harvard University where he performed a key experiment showing the outcome of crosses between lines that differ in a quantitative trait. He is also known as a critic of consumption and as a pioneer of thinking about environmental limits. While some scholars see his population thinking as nothing more than eugenics on a global scale, others see his population thinking as driven by environmental concerns, not eugenics.

<span class="mw-page-title-main">Zygosity</span> Degree of similarity of the alleles in an organism

Zygosity is the degree to which both copies of a chromosome or gene have the same genetic sequence. In other words, it is the degree of similarity of the alleles in an organism.

Genetic purging is the increased pressure of natural selection against deleterious alleles prompted by inbreeding.

The partial dominance hypothesis in genetics states that inbreeding depression is the result of the frequency increase of homozygous deleterious recessive or partially recessive alleles. The partial dominance hypothesis can be explained by looking at a population that is divided into a large number of separately inbred lines. Deleterious alleles will eventually be eliminated from some lines and become fixed in other lines, while some lines disappear because of fixation of deleterious alleles. This will cause an overall decline in population and trait value, but then increase to a trait value that is equal to or greater than the trait value in the original population. Crossing inbred lines restores fitness in the overdominance hypothesis and a fitness increase in the partial dominance hypothesis.

Inbreeding avoidance, or the inbreeding avoidance hypothesis, is a concept in evolutionary biology that refers to the prevention of the deleterious effects of inbreeding. Animals only rarely exhibit inbreeding avoidance. The inbreeding avoidance hypothesis posits that certain mechanisms develop within a species, or within a given population of a species, as a result of assortative mating and natural and sexual selection, in order to prevent breeding among related individuals. Although inbreeding may impose certain evolutionary costs, inbreeding avoidance, which limits the number of potential mates for a given individual, can inflict opportunity costs. Therefore, a balance exists between inbreeding and inbreeding avoidance. This balance determines whether inbreeding mechanisms develop and the specific nature of such mechanisms.

This glossary of genetics and evolutionary biology is a list of definitions of terms and concepts used in the study of genetics and evolutionary biology, as well as sub-disciplines and related fields, with an emphasis on classical genetics, quantitative genetics, population biology, phylogenetics, speciation, and systematics. It has been designed as a companion to Glossary of cellular and molecular biology, which contains many overlapping and related terms; other related glossaries include Glossary of biology and Glossary of ecology.

References

  1. Schnable, Patrick S.; Springer, Nathan M. (2013-04-29). "Progress Toward Understanding Heterosis in Crop Plants". Annual Review of Plant Biology. 64 (1): 71–88. doi:10.1146/annurev-arplant-042110-103827. ISSN   1543-5008. PMID   23394499.
  2. "Drought-tolerant hybrid seed offers farmers reprieve from hunger". CIMMYT. 2019-03-06. Retrieved 2023-01-19.
  3. George Harrison Shull (1948). "What Is "Heterosis"?". Genetics. 33 (5): 439–446. doi:10.1093/genetics/33.5.439. PMC   1209417 . PMID   17247290.
  4. Edmands, Suzanne (2006-11-15). "Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management: RELATIVE RISKS OF INBREEDING AND OUTBREEDING". Molecular Ecology. 16 (3): 463–475. doi:10.1111/j.1365-294X.2006.03148.x. PMID   17257106. S2CID   457825.
  5. 1 2 Ni Z, Kim ED, Ha M, et al. (January 2009). "Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids". Nature. 457 (7227): 327–31. Bibcode:2009Natur.457..327N. doi:10.1038/nature07523. PMC   2679702 . PMID   19029881.
  6. 1 2 3 4 Baranwal VK, Mikkilineni V, Zehr UB, Tyagi AK, Kapoor S (November 2012). "Heterosis: emerging ideas about hybrid vigour". J. Exp. Bot. 63 (18): 6309–14. doi: 10.1093/jxb/ers291 . PMID   23095992.
  7. Crow, James F. (1948). "Alternative Hypotheses of Hybrid Vigor". Genetics. 33 (5): 477–487. doi:10.1093/genetics/33.5.477. PMC   1209419 . PMID   17247292.
  8. Davenport CB (1908). "Degeneration, albinism and inbreeding". Science. 28 (718): 454–5. Bibcode:1908Sci....28..454D. doi:10.1126/science.28.718.454-b. PMID   17771943. S2CID   29068462.
  9. 1 2 Carr, David E.; Dudash, Michele R. (2003-06-29). "Recent approaches into the genetic basis of inbreeding depression in plants". Philosophical Transactions of the Royal Society B: Biological Sciences. 358 (1434): 1071–1084. doi:10.1098/rstb.2003.1295. ISSN   0962-8436. PMC   1693197 . PMID   12831473.
  10. East EM (1908). "Inbreeding in corn". Reports of the Connecticut Agricultural Experiments Station for 1907: 419–428.
  11. Shull GH (1908). "The composition of a field of maize". Reports of the American Breeders Association: 296–301.
  12. Birchler J.A.; Auger D.L.; Riddle N.C. (2003). "In search of the molecular basis of heterosis". The Plant Cell. 15 (10): 2236–2239. doi:10.1105/tpc.151030. PMC   540269 . PMID   14523245.
  13. 1 2 Crow, James F. (1998). "90 Years Ago: The Beginning of Hybrid Maize". Genetics. 148 (3): 923–928. doi:10.1093/genetics/148.3.923. PMC   1460037 . PMID   9539413.
  14. Han Z, Mtango NR, Patel BG, Sapienza C, Latham KE (October 2008). "Hybrid vigor and transgenerational epigenetic effects on early mouse embryo phenotype". Biol. Reprod. 79 (4): 638–48. doi:10.1095/biolreprod.108.069096. PMC   2844494 . PMID   18562704.
  15. Zhou Y, Ferguson J, Chang JT, Kluger Y (2007). "Inter- and intra-combinatorial regulation by transcription factors and microRNAs". BMC Genomics. 8: 396. doi: 10.1186/1471-2164-8-396 . PMC   2206040 . PMID   17971223.
  16. 1 2 Fort, Antoine; Ryder, Peter; McKeown, Peter C.; Wijnen, Cris; Aarts, Mark G.; Sulpice, Ronan; Spillane, Charles (2016-01-01). "Disaggregating polyploidy, parental genome dosage and hybridity contributions to heterosis in Arabidopsis thaliana". The New Phytologist. 209 (2): 590–599. doi: 10.1111/nph.13650 . ISSN   1469-8137. PMID   26395035.
  17. Duszynska, Dorota; McKeown, Peter C.; Juenger, Thomas E.; Pietraszewska-Bogiel, Anna; Geelen, Danny; Spillane, Charles (2013-04-01). "Gamete fertility and ovule number variation in selfed reciprocal F1 hybrid triploid plants are heritable and display epigenetic parent-of-origin effects". The New Phytologist. 198 (1): 71–81. doi: 10.1111/nph.12147 . ISSN   1469-8137. PMID   23368793.
  18. Wu, Shellen X. (2021-07-01). "Yuan Longping (1930–2021)". Nature. 595 (7865): 26. Bibcode:2021Natur.595...26W. doi:10.1038/d41586-021-01732-2. ISSN   0028-0836. S2CID   235633772.
  19. 1 2 3 4 Liao, Chancan; Yan, Wei; Chen, Zhufeng; Xie, Gang; Deng, Xing Wang; Tang, Xiaoyan (June 2021). "Innovation and development of the third-generation hybrid rice technology". The Crop Journal. 9 (3): 693–701. doi: 10.1016/j.cj.2021.02.003 . S2CID   233623160.
  20. 1 2 3 Kim, Yu-Jin; Zhang, Dabing (January 2018). "Molecular Control of Male Fertility for Crop Hybrid Breeding". Trends in Plant Science. 23 (1): 53–65. doi:10.1016/j.tplants.2017.10.001. PMID   29126789.
  21. O'Neill, D. G.; Church, D. B.; McGreevy, P. D.; Thomson, P. C.; Brodbelt, D. C. (2013). "Longevity and mortality of owned dogs in England" (PDF). The Veterinary Journal. 198 (3): 638–43. doi:10.1016/j.tvjl.2013.09.020. PMID   24206631.
  22. Spady, Tyrone C.; Ostrander, Elaine A. (2008). "Canine Behavioral Genetics: Pointing Out the Phenotypes and Herding up the Genes". American Journal of Human Genetics. 82 (1): 10–8. doi:10.1016/j.ajhg.2007.12.001. PMC   2253978 . PMID   18179880.
  23. John Paul Scott and John L. Fuller. "Genetics and the Social Behavior of the Dog". 1965. p. 307 and p. 313.
  24. Per Jensen. "The Behavioural Biology of Dogs". 2007. p. 179
  25. Nicholas, Frank W (2016). "Hybrid vigour in dogs?". Veterinary Journal. 214: 77–83. doi:10.1016/j.tvjl.2016.05.013. PMID   27387730 . Retrieved 29 July 2020.
  26. Nicholas, J A C (2012). "Survey of ophthalmic abnormalities in the labradoodle in the UK". The Veterinary Record. 170 (15): 390. doi:10.1136/vr.100361. PMID   22278634. S2CID   5932838 . Retrieved 29 July 2020.
  27. Sharkey, Laura (2020). "Hybrid Vigor in Dogs". The Functional Dog Collaborative. Retrieved 29 July 2020.
  28. Australian Geographic (September 2014). "Hybrid birds better at fighting disease than purebreds".
  29. Hawks, John (2013). Significance of Neandertal and Denisovan Genomes in Human Evolution. Vol. 42. Annual Reviews. pp. 433–449, 438. doi:10.1146/annurev-anthro-092412-155548. ISBN   978-0-8243-1942-7. ISSN   0084-6570. The shared evolutionary history of living humans has resulted in a high relatedness among all living people, as indicated for example by the very low fixation index (FST) among living human populations.{{cite book}}: |journal= ignored (help)
  30. Barbujani, Guido; Colonna, Vincenza (15 September 2011). "Genetic Basis of Human Biodiversity: An Update". In Zachos, Frank E.; Habel, Jan Christian (eds.). Biodiversity Hotspots. Springer. pp. 97–119. doi:10.1007/978-3-642-20992-5_6. ISBN   978-3-642-20992-5 . Retrieved 23 November 2013. The massive efforts to study the human genome in detail have produced extraordinary amounts of genetic data. Although we still fail to understand the molecular bases of most complex traits, including many common diseases, we now have a clearer idea of the degree of genetic resemblance between humans and other primate species. We also know that humans are genetically very close to each other, indeed more than any other primates, that most of our genetic diversity is accounted for by individual differences within populations, and that only a small fraction of the species' genetic variance falls between populations and geographic groups thereof.
  31. Ramachandran, Sohini; Tang, Hua; Gutenkunst, Ryan N.; Bustamante, Carlos D. (2010). "Genetics and Genomics of Human Population Structure". In Speicher, Michael R.; Antonarakis, Stylianos E.; Motulsky, Arno G. (eds.). Vogel and Motulsky's Human Genetics. Heidelberg: Springer Scientific. pp. 589–615. doi:10.1007/978-3-540-37654-5_22. ISBN   978-3-540-37653-8. S2CID   89318627. Most studies of human population genetics begin by citing a seminal 1972 paper by Richard Lewontin bearing the title of this subsection [29]. Given the central role this work has played in our field, we will begin by discussing it briefly and return to its conclusions throughout the chapter. ... A key conclusion of the paper is that 85.4% of the total genetic variation observed occurred within each group. That is, he reported that the vast majority of genetic differences are found within populations rather than between them. ... His finding has been reproduced in study after study up through the present: two random individuals from any one group (which could be a continent or even a local population) are almost as different as any two random individuals from the entire world
  32. Kamin, Leon J. (1980). "Inbreeding depression and IQ". Psychological Bulletin. 87 (3): 469–478. doi:10.1037/0033-2909.87.3.469. ISSN   1939-1455. PMID   7384341.
  33. 1 2 Risch N, Burchard E, Ziv E, Tang H (July 2002). "Categorization of humans in biomedical research: genes, race and disease". Genome Biol. 3 (7): comment2007. doi: 10.1186/gb-2002-3-7-comment2007 . PMC   139378 . PMID   12184798.
  34. Weller SG, Sakai AK, Thai DA, Tom J, Rankin AE (November 2005). "Inbreeding depression and heterosis in populations of Schiedea viscosa, a highly selfing species". J. Evol. Biol. 18 (6): 1434–44. doi: 10.1111/j.1420-9101.2005.00965.x . PMID   16313456.

Further reading