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Outbreeding depression

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The outcome of breeding after a population has diverged, resulting in outbreeding depression

In biology, outbreeding depression happens when crosses between two genetically distant groups or populations result in a reduction of fitness.[1] This is particularly likely if the subspecies have different habitats or if no genetic exchange has occurred, except in the distant past.[2] The concept is in contrast to inbreeding depression, although the two effects can occur simultaneously.[3] The risks of outbreeding are on par with the risks of inbreeding,[4] and these risks sometimes limits the potential for genetic rescue or augmentations.[1] Indeed, studies that report hybridization in mammals find resulting negative consequences about 4 times more likely than positive consequences.[5] Outbreeding depression can occur between an invasive population and a native populations; hybridization can result in extinction of the native species[6] or the loss of native adaptations.[7] Outbreeding depression considered post-zygotic response because outbreeding depression is noted usually in the performance of the progeny.[8]

Outbreeding depression manifests in two ways:

  • Generating intermediate genotypes that are less fit than either parental form. For example, selection in one population might favor a large body size, whereas in another population small body size might be more advantageous, while individuals with intermediate body sizes are comparatively disadvantaged in both populations. As another example, in the Tatra Mountains, the introduction of ibex from the Middle East resulted in hybrids which produced calves at the coldest time of the year.[9]
  • Breakdown of biochemical or physiological compatibility. Within isolated breeding populations, alleles are selected in the context of the local genetic background. Because the same alleles may have rather different effects in different genetic backgrounds, this can result in different locally coadapted gene complexes. Outcrossing between individuals with differently adapted gene complexes can result in disruption of this selective advantage, resulting in a loss of fitness.

Mechanisms for generating outbreeding depression

The different mechanisms of outbreeding depression can operate at the same time. However, determining which mechanism is likely to occur in a particular population can be very difficult.

There are three main mechanisms for generating outbreeding depression:

  1. Fixed chromosomal differences resulting in the partial or complete sterility of F1 hybrids.[1]
  2. Adaptive differentiation among populations
  3. Population bottlenecks and genetic drift

The first mechanism for generating outbreeding depression has the greatest effects on fitness for polyploids, an intermediate effect on translocations, and a modest effect on centric fusions and inversions.[1] Generally this mechanism will be more prevalent in the first generation (F1) after the initial outcrossing when most individuals are made up of the intermediate phenotype. Some mechanisms may not appear until two or more generations later (F2 or greater),[10] when recombination has undermined vitality of positive epistasis. Hybrid vigor in the first generation can, in some circumstances, be strong enough to mask the effects of outbreeding depression. An example of this is that plant breeders will make F1 hybrids from purebred strains, which will improve the uniformity and vigor of the offspring, however the F2 generation are not used for further breeding because of unpredictable phenotypes in their offspring. Unless there is strong selective pressure, outbreeding depression can increase in further generations as coadapted gene complexes are broken apart without the forging of new coadapted gene complexes to take their place. If the outcrossing is limited and populations are large enough, selective pressure acting on each generation can restore fitness. Unless the F1 hybrid generation is sterile or very low fitness, selection will act in each generation using the increased diversity to adapt to the environment.[11] This can lead to recovery in fitness to baseline, and sometimes even greater fitness than original parental types in that environment.[12] However, as the hybrid population will likely to go through a decline in fitness for a few generations, they will need to persist long enough to allow selection to act before they can rebound.[3]

Effects on species

Outbreeding depression has a large effect on conservation efforts in addition to human-generated or other forms of wildlife disruption in which locally adapted organisms move into "new habitats where they can interbreed with resident organisms."[13] This should be considered a risk for conservation "even when the degree of genetic divergence" between populations "is small."[13] The native genotypes of parental unmixed populations have complex local adaptations across many loci that can disappear through within-species hybridization, so increasing genetic exchange between these populations could be harmful.[14] Hybridization is causing extinction of many species and subspecies by both "replacement and genetic mixing."[14] Outbreeding risks can be minimized by hybridizing "only for populations clearly suffering from inbreeding depression, maximizing the genetic and adaptive similarity between populations, and testing the effects of hybridization for at least two generations whenever possible."[4]

Mixing stocks of bass (largemouth bass and its closest relative, Florida bass) reduced fitness by 50%,[15] and the author posits that the mixing of Florida and largemouth bass is contributing to an ongoing viral bass infection epidemic.[13]

Outbreeding depression due to interbreeding of rainbow trout populations resulted in decreased ability to fend off a parasitic infection in the wild.[16]

Two German species of mice have a small overlapping range where interbreeding can occur. Interbred mice have ~10x more parasites than non-interbred mice. These mice are very susceptible to parasitism likely because the different populations have different genes for resistance, so recombinant crosses lose any ability of resistance.[17]

The mallard duck interbreeding is associated with population decline in the New Zealand gray duck, the Florida mottled duck (threatening the species' existence), Australian black duck, and the endangered Hawaiian duck, hampering conservation efforts. Introgression also threatens the existence other types of duck species, dove species, owl species, multiple other bird species, cat species, wolf species, ferret species, deer, mink, horse, frog species, various fish species, and many plant species.[6][14]

These deleterious effects can be avoided by preventing hybridization between animal populations with different coadapted complexes.[18]

In animals

Edmands et al. (2007) lists 35 within-species crosses that resulted in outbreeding depression "in a diversity of plants, invertebrates and vertebrates." Incompatibility between two populations leading to outbreeding depression evolves more quickly in mammals than birds, and plants even more slowly than either.[4]

Vertebrates

Outbreeding depression may be more frequent in vertebrates than was previously thought.[19][14] Two populations of pink salmon (Oncorhynchus gorbuscha) that were separated by about 600 miles, and the offspring of the two populations exhibited decreased survival in the F2 generation compared to either parental generation.

Two populations of largemouth bass (Micropterus salmoides) were crossed, and the F2 generation suffered from a breakdown of coadapted gene complexes in their immune systems, which resulted in a 3.6 times higher rate of mortality from infection and an decrease in fitness compared to the native parental populations. Notably, these populations were of the same species and "have undergone only a small degree of genetic differentiation."[13]

Examples of outbreeding depression generated from adaptive differentiation include stickleback fish, which developed benthic and limnetic forms when separated. When crosses occurred between the two forms, there were low spawning rates. However, when the same forms mated with each other and no crossing occurred between lakes, the spawning rates were normal. Outbreeding depression caused by genetic drift has affected poison dart frogs, anole lizards, and cichlid fish.[1]

Outbreeding depression has been observed in mice.[17]

Banes et al. (2016) suggests the possibility that some Bornean orangutans have experienced outbreeding depression due to a cross with other orangutan subspecies, as the subspecies diverged 176,000 years ago, much greater than the 500-year or 20-generation[1] isolation benchmark.[20]

Neanderthal genes in modern humans have been strongly selected against, especially genes that are on the X chromosome or are active in male germ cells, suggesting that human-Neanderthal hybrids were less fertile.[21]

Invertebrates

Tigriopus californicus tends to stay in one area because leaving its native habitat is genetically costly due to significant outbreeding depression, while staying in its native pool is not genetically detrimental. Fitness was reduced when an individuals from different areas mated.[22]

The fruit-fly Drosophila montana exhibited outbreeding depression (lower fitness than either parental population) due to decreased success mating.[23] Lower spawn rates than either parental population has been observed in Drosophila as well as leaf beetles, where the F1 progeny and later progeny resulted in intermediate fitness between the two parents. This circumstance is more likely to happen and occurs more quickly with selection than with genetic drift.[1] Another study in beetles found that incestuous matings did not result in a reduction of fitness among progeny, but matings between different populations within the same species did result in decreased fitness: outbreeding depression, but not inbreeding depression, occurred.[24]

In plants

For plants, outbreeding depression represents a partial crossing barrier.[8] Unfortunately, outbreeding depression is not understood well in angiosperms. After observing Ipomopsis aggregata over time by crossing plants that were between 10–100m apart, a pattern was noticed that plants that were farther away spatially had a higher likelihood of outbreeding depression.[8] Some general takeaways from this were that spatial patterns of selection on plant genotypes will vary in scale and pattern, and outbreeding depression reflects the genetic constitution of "hybrid" progeny and the environments in which the parents and progeny grow.[8] This means that although outbreeding depression cannot be predicted in angiosperms yet, the environment has a role in it. Mating between individuals over a distance of only 30 meters in Delphinium nelsonii caused a 48% reduction in F1 body size.[25]

See also

References

Public Domain This article incorporates public domain material from Michael Lynch. Inbreeding depression and outbreeding depression. National Park Service.
  1. ^ a b c d e f g Frankham, Richard; Ballou, Jonathan D.; Eldridge, Mark D. B.; Lacy, Robert C.; Ralls, Katherine; Dudash, Michele R.; Fenster, Charles B. (June 2011). "Predicting the probability of outbreeding depression". Conservation Biology: The Journal of the Society for Conservation Biology. 25 (3): 465–475. doi:10.1111/j.1523-1739.2011.01662.x. ISSN 1523-1739. PMID 21486369. S2CID 14824257.
  2. ^ Banes, Graham L.; Galdikas, Biruté M. F.; Vigilant, Linda (2016-02-25). "Reintroduction of confiscated and displaced mammals risks outbreeding and introgression in natural populations, as evidenced by orang-utans of divergent subspecies". Scientific Reports. 6 (1): 22026. doi:10.1038/srep22026. ISSN 2045-2322. PMC 4766574. PMID 26911345.
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  13. ^ a b c d Goldberg, Tony L.; Grant, Emily C.; Inendino, Kate R.; Kassler, Todd W.; Claussen, Julie E.; Philipp, David P. (April 2005). "Increased Infectious Disease Susceptibility Resulting from Outbreeding Depression". Conservation Biology. 19 (2): 455–462. doi:10.1111/j.1523-1739.2005.00091.x. ISSN 0888-8892. S2CID 17063955.
  14. ^ a b c d Allendorf, Fred W.; Leary, Robb F.; Spruell, Paul; Wenburg, John K. (2001-11-01). "The problems with hybrids: setting conservation guidelines". Trends in Ecology & Evolution. 16 (11): 613–622. doi:10.1016/S0169-5347(01)02290-X. ISSN 0169-5347.
  15. ^ Black bass : ecology, conservation, and management : proceedings of the symposium black bass 2000--ecology, conservation, and management of black bass in North America, held at St. Louis, Missouri, USA, 21-24 August 2000. David P. Philipp, Mark Stephen Ridgway. Bethesda, Md.: American Fisheries Society. 2002. ISBN 1-888569-38-7. OCLC 51651181.{{cite book}}: CS1 maint: others (link)
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  23. ^ Doty, Lewis (2022-07-19). "Outbreeding depression - Genetic Diversity". Ecology Center. Retrieved 2022-07-22.
  24. ^ Peer, Katharina; Taborsky, Michael (2005). "Outbreeding Depression, but No Inbreeding Depression in Haplodiploid Ambrosia Beetles with Regular Sibling Mating". Evolution. 59 (2): 317–323. doi:10.1111/j.0014-3820.2005.tb00992.x. ISSN 0014-3820. JSTOR 3448923. PMID 15807418. S2CID 17528068.
  25. ^ Waser, Nickolas M.; Price, Mary V. (1989). "Optimal Outcrossing in Ipomopsis aggregata: Seed Set and Offspring Fitness". Evolution. 43 (5): 1097–1109. doi:10.2307/2409589. ISSN 0014-3820. JSTOR 2409589. PMID 28564159.
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