Genetic incompatibility

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Genetic incompatibility describes the process by which mating yields offspring that are nonviable, prone to disease, or genetically defective in some way. In nature, animals can ill afford to devote costly resources for little or no reward, ergo, mating strategies have evolved to allow females to choose or otherwise determine mates which are more likely to result in viable offspring.

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Polyandry, for instance, when a female mates with two or more males during a period of sexual receptivity, reduces the chance that a singular mate is genetically incompatible. Exactly how females determine compatible genes prior to mating is not completely understood, but various mechanisms have been proposed, such as pheromones and male appearance and/or courtship behavior.

It is also surmised that sexual selection can continue after copulation, the so called 'cryptic female choice', so named because it takes place within the body and cannot be directly observed. In this scenario, incompatible male sperm can be rejected by the female.

Genetic incompatibility can be engineered by scientists in order to control pests such as mosquitos and fruit flies.

Infertility

Introduced to the scientific community in the early 1990s, the concept of cryptic female choice is complicated and offers a new explanation for infertility. [1] Non-additive genetic effects have been thought of to be the main reason for reproductive isolation between species. [2] More recent studies have concluded that in comparison to additive genetic effects, non-additive genetic effects have a more important role in fertility and embryo survival. [2] [3] [4] [5] [6] As a result, some scientists have concluded that rather than the genes of the female alone or the genes of the male alone being the reason for the pair to be infertile, it is a result of the relationship and compatibility of their genes. [2] Thus, some male genotypes may have a higher success rate of fertilization with some female genotypes rather than others. [2]

Certain alleles being paired together can lead to complete reproductive failure/incompatibility as a result of differential compatibility between different variants. [2] Another contributing factor to incompatibility is based on the surface carbohydrates of the gametes. [2] Multiple studies have shown that the physical contact between the sperm and the egg can cause a chemical reaction in the female. [2] This reaction occurs when the egg comes in contact with non-compatible surface glycans and can impact the sperm's potential for fertilization by causing structural changes in the sperm's surface glycans. [2]

Fruit flies

There are numerous other factors that can likewise contribute to the incompatibility of male and female haplotypes within an embryo. [7] For example, certain male Drosophila melanogaster (Fruit Flies) carry a drive allele that on average results in them producing 50% less viable sperm than their counterparts who are not heterozygous for the allele. [7] Not only are offspring of heterozygous males less genetically competitive, if both the male and female are heterozygous, their offspring will be either inviable or infertile [7]

Rosy bitterlings

Rhodeus ocellatus Rhodeus ocellatus ocellatus-m.JPG
Rhodeus ocellatus

One example of how indirect non additive genes impact fertility comes from a team of researchers who investigated how female rhodeus ocellatus (rosy bitterlings) employ mate choice and the role of the MHC gene in that decision. [3] After allowing females and males to mate, they collected DNA from all the adult bitterlings as well as their offspring. [3] The data showed that females were more likely to choose males whose MHC gene was dissimilar to theirs. [3] The offspring that came from a pair who had dissimilar MHC genes had higher survival rates. [3] Although these researchers did not test this theory, they speculated that perhaps during the male's courtship, he dissipates odor cues from the MHC gene that assist the female in her decision-making process [3]

Mice

DDK is a lethal phenotype in Mus Domesticus (house mice) that leads to developmental abnormalities and eventually deterioration of the embryo when females with the phenotype mate with males who carry other inbred strains. [8] Scientists have discovered that expression of this incompatibility within the embryo depends on the paternal allele of the DDK syndrome. [8] If the paternal allele is compatible, meaning the male is not carrying an inbred strain (ex. DDK female x non-DDK male), the embryo will survive. [8] However if the male carries the incompatible allele, the embryo will not survive. [8]

Sympatric color morphs

Genetic color polymorphisms are genetically defined color forms between animals of the same species. [9] For the most part, color morphs within a population can interbreed without any issues. However, evidence shows that in certain cases, the viability of interbred color morph offspring is drastically lower than those that present the same color. [9] While coloration is the most pronounced exhibition of a certain phenotype as individuals can be easily and quickly differentiated to the human eye, there are other factors that may be affected but not as easily identified. [10]

Gouldian finches

Erythrura Gouldiae GouldianFinches.jpg
Erythrura Gouldiae

A group of researchers investigated how the survival rates of offspring of Erythrura Gouldiae (Gouldian finch) are impacted when the mating pair have genes for different colors. [9] They bred both pure and mixed pairs of the finches (in this species the gene for producing a red-headed finch is dominant to the one that produces a black headed finch). [9] After incubation, eggs that were produced from mixed pairs were 34.3% less likely to hatch compared to those that were produced from pure pairs. [9] The mixed-pair offspring that did survive the incubation stage were still at a disadvantage, being burdened with a 32.1% increase in mortality between the time that they hatched and 60 days after (during which time they were still in the care of parents). [9] Even after becoming independent, the offspring mortality of mixed pairs was still higher. Specifically the rate of mortality of daughters from mixed-genotypes was much higher. [9]

Female polyandry and genetic incompatibility

Polyandry is a mating pattern that is identified in species when a female mates with two or more males during a period of sexual receptivity. [11] Females may engage in this behavior in the event that their singular mate is a genetically incompatible match. [12] If that were to be the case, she would lose the chance to become pregnant during that season and not be able to try again until the next mating window. [12]

Creating offspring requires the female to allocate a large portion of her resources to both the formation of the embryo. [7] Partaking in polyandry allows her to ensure that the offspring that she will be providing for is going to be viable, and not be a waste of her time, energy, and resources. [7]

Another experiment was done with Gouldian finches, during which researchers wanted to determine the effect of compatibility and incompatibility on the relationship between socially monogamous pairs of finches. [13] They discovered that by participating in "extra-pair" mating relationships, the females were able to more accurately target compatible genes, thus increasing the amount of viable offspring that they produce. [13] Researchers paired females with both compatible and incompatible males as their social partner. However, they also made available both compatible and incompatible males as the extra-pair partner. [13] The data collected revealed that 77.5% of the females mated outside of their pairs. If their extra-pair was compatible (unlike their social partner), the female experienced a 38.9% increase in offspring survival. [13] Although females are unable to tell the difference between compatible and incompatible partners, by participating in polyandry, their likelihood of yielding more and healthier offspring is increased. [13]

Selfish genetic elements

Mus Domesticus Mus-musculus-in-nature.JPG
Mus Domesticus

Selfish genetic elements are genes that will use various methods to ensure that they are transferred on to new generations. [14] Selfish elements have the potential to create genetic incompatibilities because their effects frequently depend on interactions with the host genotype and according to whether selfish elements are present in both parents. [15] There has been some debate over whether these selfish genetic elements can actually influence the post-copulatory sperm selection that some females go through in order to determine the best (most compatible) match for her genes. [14]

Mice, carry a particular type of selfish genetic element known as a segregation distorter. [16] This specific classification is able to establish themselves in over 50% of offspring after the meiosis period. [16] Specific to mice, the distorter that they can carry is known as the t-complex. [17] This specific allele is recessive lethal, meaning that it can have a serious effect on the fitness of offspring as well and is most likely deadly. [17] After multiple experiments, it was found that both males and females will avoid mating with those of the opposite sex who are heterozygous for the allele but showed a strong preference for those that were not carriers of the allele. [17] If they were to mate with a heterozygous partner, it could potentially lead to half of their offspring dying as a result of the lethal allele [17]

Engineered genetic incompatibility

Engineered Genetic Incompatibility (EGI) is a technique that is being developed to manufacture incompatibility between species in order to aid in population suppression. [18] Mimicking the Sterile Insect Technique, by introducing EGI males into a population, a sex-sorting incompatible male system is generated. [18] Males that have been genetically modified are able to compete for the attention of females at the same level as those that have not been modified. [18] Because the EGI males are equal rivals to their wild counterparts, they are able to use the female's time and energy reproducing but only to create non-viable offspring. [18]

Drosophila Melanogaster Fruit-flies-red-and-white-eyes.jpg
Drosophila Melanogaster

A team of researchers from the University of Minnesota were successful in genetically engineering a population of fruit flies that would not be able to generate viable progeny when mating with wild-types specifically. [18] The researchers manufactured flies that would express a dCas9-based programmable transcription activator or PTA. [18] By this method, the promoter of any gene could be affected. [18] When the EGI flies mate with each other, they are able to avoid the negative effects the PTA generates because they were also given the gene for a mutation that could combat the overexpression of the gene. [18] Their offspring would go on to carry the same incompatibilities to the next generation, furthering the impact on the population. [18] However, the offspring that are produced by hybrid pairs (one EGI and one wild type) have a heterozygous pair of both the PTA and resistance genes and do not survive long after hatching, if they ever do as a result of the PTA's disabling effect on the gene promoter. [18]

Mosquitoes

Aedes aegypti Aedes aegypti.jpg
Aedes aegypti

A great deal of research has gone into trying to use this technology as a tool in order to try and control the spread of diseases that are carried by mosquitoes such as Dengue, Zika, and Chikungunya. [19] Because of the successful research done on fruit flies, a team of researchers was able to manipulate some aspects of the experiment and effectively control a simulated population of Aedes aegypti (mosquitoes). [19] For their experiment, they used female lethality meaning that the engineered female mosquitoes will not survive the initial stages of their lives. [19] The researchers titled this new approach the Self-Sorting Incompatible Male System (SSIMS). [19] They observed an increase in population suppression as they increased the number of SSIMS mosquitoes released because the offspring conceived from the SSIMS males were inviable. [19] After this success, a new strategy was modeled, Field-Amplified Male Sterility System (FAMSS). [19] This led to an even bigger impact on population control as the offspring were viable but sterile. [19]

Related Research Articles

An allele, or allelomorph, is a variant of the sequence of nucleotides at a particular location, or locus, on a DNA molecule.

Disassortative mating is a mating pattern in which individuals with dissimilar phenotypes mate with one another more frequently than would be expected under random mating. Disassortative mating reduces the mean genetic similarities within the population and produces a greater number of heterozygotes. The pattern is character specific, but does not affect allele frequencies. This nonrandom mating pattern will result in deviation from the Hardy-Weinberg principle.

<span class="mw-page-title-main">Haldane's rule</span> Observation in evolutionary biology

Haldane's rule is an observation about the early stage of speciation, formulated in 1922 by the British evolutionary biologist J. B. S. Haldane, that states that if — in a species hybrid — only one sex is inviable or sterile, that sex is more likely to be the heterogametic sex. The heterogametic sex is the one with two different sex chromosomes; in therian mammals, for example, this is the male.

A mating system is a way in which a group is structured in relation to sexual behaviour. The precise meaning depends upon the context. With respect to animals, the term describes which males and females mate under which circumstances. Recognised systems include monogamy, polygamy, and promiscuity, all of which lead to different mate choice outcomes and thus these systems affect how sexual selection works in the species which practice them. In plants, the term refers to the degree and circumstances of outcrossing. In human sociobiology, the terms have been extended to encompass the formation of relationships such as marriage.

Intragenomic conflict refers to the evolutionary phenomenon where genes have phenotypic effects that promote their own transmission in detriment of the transmission of other genes that reside in the same genome. The selfish gene theory postulates that natural selection will increase the frequency of those genes whose phenotypic effects cause their transmission to new organisms, and most genes achieve this by cooperating with other genes in the same genome to build an organism capable of reproducing and/or helping kin to reproduce. The assumption of the prevalence of intragenomic cooperation underlies the organism-centered concept of inclusive fitness. However, conflict among genes in the same genome may arise both in events related to reproduction and altruism.

<span class="mw-page-title-main">Haplodiploidy</span> Biological system where sex is determined by the number of sets of chromosomes

Haplodiploidy is a sex-determination system in which males develop from unfertilized eggs and are haploid, and females develop from fertilized eggs and are diploid. Haplodiploidy is sometimes called arrhenotoky.

The mechanisms of reproductive isolation are a collection of evolutionary mechanisms, behaviors and physiological processes critical for speciation. They prevent members of different species from producing offspring, or ensure that any offspring are sterile. These barriers maintain the integrity of a species by reducing gene flow between related species.

<span class="mw-page-title-main">Sexual conflict</span> Term in evolutionary biology

Sexual conflict or sexual antagonism occurs when the two sexes have conflicting optimal fitness strategies concerning reproduction, particularly over the mode and frequency of mating, potentially leading to an evolutionary arms race between males and females. In one example, males may benefit from multiple matings, while multiple matings may harm or endanger females, due to the anatomical differences of that species. Sexual conflict underlies the evolutionary distinction between male and female.

Extra-pair copulation (EPC) is a mating behaviour in monogamous species. Monogamy is the practice of having only one sexual partner at any one time, forming a long-term bond and combining efforts to raise offspring together; mating outside this pairing is extra-pair copulation. Across the animal kingdom, extra-pair copulation is common in monogamous species, and only a very few pair-bonded species are thought to be exclusively sexually monogamous. EPC in the animal kingdom has mostly been studied in birds and mammals. Possible benefits of EPC can be investigated within non-human species, such as birds.

<span class="mw-page-title-main">Mate choice</span> One of the primary mechanisms under which evolution can occur

Mate choice is one of the primary mechanisms under which evolution can occur. It is characterized by a "selective response by animals to particular stimuli" which can be observed as behavior. In other words, before an animal engages with a potential mate, they first evaluate various aspects of that mate which are indicative of quality—such as the resources or phenotypes they have—and evaluate whether or not those particular trait(s) are somehow beneficial to them. The evaluation will then incur a response of some sort.

<i>Stegodyphus lineatus</i> Species of spider

Stegodyphus lineatus is the only European species of the spider genus Stegodyphus. Male S. lineatus can grow up to 12 mm long while females can grow up to 15 mm. The colour can range from whitish to almost black. In most individuals the opisthosoma is whitish with two broad black longitudinal stripes. Males and females look similar, but the male is generally richer in contrast and has a bulbous forehead. The species name refers to the black lines on the back of these spiders. S. lineatus is found in the southern Mediterranean region of Europe and as far east as Tajikistan.

<span class="mw-page-title-main">Parthenogenesis</span> Asexual reproduction without fertilization

Parthenogenesis is a natural form of asexual reproduction in which growth and development of an embryo occur directly from an egg, without need for fertilization. In animals, parthenogenesis means development of an embryo from an unfertilized egg cell. In plants, parthenogenesis is a component process of apomixis. In algae, parthenogenesis can mean the development of an embryo from either an individual sperm or an individual egg.

<span class="mw-page-title-main">Sexy son hypothesis</span> Postulate in biology

The sexy son hypothesis in evolutionary biology and sexual selection, proposed by Patrick J. Weatherhead and Raleigh J. Robertson of Queen's University in Kingston, Ontario in 1979, states that a female's ideal mate choice among potential mates is one whose genes will produce males with the best chance of reproductive success. This implies that other benefits the father can offer the mother or offspring are less relevant than they may appear, including his capacity as a parental caregiver, territory and any nuptial gifts. Fisher's principle means that the sex ratio is always near 1:1 between males and females, yet what matters most are her "sexy sons'" future breeding successes, more likely if they have a promiscuous father, in creating large numbers of offspring carrying copies of her genes. This sexual selection hypothesis has been researched in species such as the European pied flycatcher.

<i>Drosophila pseudoobscura</i> Species of fly

Drosophila pseudoobscura is a species of fruit fly, used extensively in lab studies of speciation. It is native to western North America.

<span class="mw-page-title-main">Red flour beetle</span> Species of beetle

The red flour beetle is a species of beetle in the family Tenebrionidae, the darkling beetles. The red flour beetle, and other closely related beetles like the Gnatocerus cornutus, are a worldwide pest of stored products, particularly food grains, and a model organism for ethological and food safety research.

<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 matchmaking is the idea of matching couples for romantic relationships based on their biological compatibility. The initial idea was conceptualized by Claus Wedekind through his "sweaty t-shirt" experiment. Males were asked to wear T-shirts for two consecutive nights, and then females were asked to smell the T-shirts and rate the body odors for attractiveness. Human body odor has been associated with the human leukocyte antigens (HLA) genomic region. They discovered that females were attracted to men who had dissimilar HLA alleles from them. Furthermore, these females reported that the body odors of HLA-dissimilar males reminded them of their current partners or ex-partners providing further evidence of biological compatibility.

<span class="mw-page-title-main">Major histocompatibility complex and sexual selection</span> Adaptive immune gene selection

The major histocompatibility complex in sexual selection concerns how major histocompatibility complex (MHC) molecules allow for immune system surveillance of the population of protein molecules in a host's cells. In 1976, Yamazaki et al. demonstrated a sexual selection mate choice by male mice for females of a different MHC.

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.

<span class="mw-page-title-main">Polyandry in animals</span> Class of mating system in non-human species

In behavioral ecology, polyandry is a class of mating system where one female mates with several males in a breeding season. Polyandry is often compared to the polygyny system based on the cost and benefits incurred by members of each sex. Polygyny is where one male mates with several females in a breeding season . A common example of polyandrous mating can be found in the field cricket of the invertebrate order Orthoptera. Polyandrous behavior is also prominent in many other insect species, including the red flour beetle, the adzuki bean weevil, and the species of spider Stegodyphus lineatus. Polyandry also occurs in some primates such as marmosets, mammal groups, the marsupial genus' Antechinus and bandicoots, around 1% of all bird species, such as jacanas and dunnocks, insects such as honeybees, and fish such as pipefish.

References

  1. ↑ Løvlie, Hanne (2016). "Cryptic Female Choice". Evolutionary Biology. doi:10.1093/OBO/9780199941728-0071. ISBN   978-0-19-994172-8.
  2. 1 2 3 4 5 6 7 8 Kekäläinen, Jukka (18 November 2021). "Genetic incompatibility of the reproductive partners: an evolutionary perspective on infertility". Human Reproduction. 36 (12): 3028–3035. doi:10.1093/humrep/deab221. PMC   8600657 . PMID   34580729.
  3. 1 2 3 4 5 6 Agbali, Muna; Reichard, Martin; Bryjová, Anna; Bryja, Josef; Smith, Carl (June 2010). "Mate Choice for Nonadditive Genetic Benefits Correlate with MHC Dissimilarity in the Rose Bitterling (Rhodeus Ocellatus)". Evolution. 64 (6): 1683–1696. doi: 10.1111/j.1558-5646.2010.00961.x . PMID   20148959. S2CID   27918567.
  4. ↑ Palucci, Valentina; Schaeffer, Lawrence R.; Miglior, Filippo; Osborne, Vern (April 2007). "Non-additive genetic effects for fertility traits in Canadian Holstein cattle (Open Access publication )". Genetics Selection Evolution. 39 (2): 181–193. doi: 10.1186/1297-9686-39-2-181 . PMC   2682836 . PMID   17306200. S2CID   13790033.
  5. ↑ Dziminski, Martin A.; Roberts, J. Dale; Simmons, Leigh W. (April 2008). "Fitness consequences of parental compatibility in the frog Crinia georgiana". Evolution. 62 (4): 879–886. doi:10.1111/j.1558-5646.2008.00328.x. PMID   18208566. S2CID   27154568.
  6. ↑ Rodríguez-Muñoz, Rolando; Tregenza, Tom (23 April 2009). "Genetic compatibility and hatching success in the sea lamprey (Petromyzon marinus)". Biology Letters. 5 (2): 286–288. doi:10.1098/rsbl.2008.0650. PMC   2665819 . PMID   19049954.
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  9. 1 2 3 4 5 6 7 Pryke, Sarah R.; Griffith, Simon C. (March 2009). "Postzygotic Genetic Incompatibility Between Sympatric Color Morphs". Evolution. 63 (3): 793–798. doi: 10.1111/j.1558-5646.2008.00584.x . PMID   19087185. S2CID   24657339.
  10. ↑ McLean, Claire A.; Stuart-Fox, Devi (November 2014). "Geographic variation in animal colour polymorphisms and its role in speciation". Biological Reviews. 89 (4): 860–873. doi:10.1111/brv.12083. PMID   24528520. S2CID   4664660.
  11. ↑ Hoogland, John L.; Trott, Regina; Keller, Stephen R. (19 February 2019). "Polyandry and Polygyny in a Social Rodent: An Integrative Perspective Based on Social Organization, Copulations, and Genetics". Frontiers in Ecology and Evolution. 7. doi: 10.3389/fevo.2019.00003 .
  12. 1 2 "The evolution of polyandry I: intragenomic conflict and genetic incompatibility". Proceedings of the Royal Society of London. Series B: Biological Sciences. 263 (1377): 1711–1717. 22 December 1996. doi:10.1098/rspb.1996.0250. S2CID   84171994.
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  15. ↑ Tregenza, T.; Wedell, N. (August 2000). "Genetic compatibility, mate choice and patterns of parentage: Invited Review". Molecular Ecology. 9 (8): 1013–1027. Bibcode:2000MolEc...9.1013T. doi: 10.1046/j.1365-294x.2000.00964.x . PMID   10964221. S2CID   9367945.
  16. 1 2 Price, Tom A. R.; Wedell, Nina (September 2008). "Selfish genetic elements and sexual selection: their impact on male fertility". Genetica. 134 (1): 99–111. doi:10.1007/s10709-008-9253-y. PMID   18327647. S2CID   20975113.
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  18. 1 2 3 4 5 6 7 8 9 10 Upadhyay, Ambuj; Feltman, Nathan R; Sychla, Adam; Janzen, Anna; Das, Siba R; Maselko, Maciej; Smanski, Michael (2 February 2022). "Genetically engineered insects with sex-selection and genetic incompatibility enable population suppression". eLife. 11. doi: 10.7554/eLife.71230 . PMC   8860436 . PMID   35108195.
  19. 1 2 3 4 5 6 7 Maselko, Maciej; Heinsch, Stephen; Das, Siba; Smanski, Michael J. (7 May 2018). Genetic incompatibility combined with female-lethality is effective and robust in simulations of Aedes aegypti population control (Preprint). doi:10.1101/316406. S2CID   90799017.
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