Inbreeding depression
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Inbreeding depression is the reduction in fitness of the offspring of related parents, measured against the offspring of unrelated parents.[1] Inbred plants and animals survive less well and are less fertile.[2] Inbreeding raises homozygosity. Most of the loss is attributed to recessive or partially recessive deleterious alleles that homozygosity exposes. Part of it may come from the loss of heterozygotes at loci where they are fitter than either homozygote.[3] Selection can remove some of the first kind of load, a process called purging.[3] Plant species that mainly outcross show more depression on average than species that mainly self.[4]
Cannabis is pollinated by the wind and is mostly dioecious and outcrossing.[5] Selfed lines of hemp and of other cannabis have lost height, biomass and flower or seed yield and have set more abnormal flowers.[6][7][5] The size of the loss varies. After 12 generations of selfing, the seed yield of a Ukrainian monoecious cultivar was 74.9 per cent below that of its starting plants, while one generation of selfing did not lower the flower yield of the Thai landrace Hang Kra Rok.[7][8] The ways cannabis is selfed are described under outcrossing and inbred line. The recovery of vigour in crosses is described under heterosis.
Measuring the loss
Inbreeding depression is measured by raising inbred and outbred progeny of one population in the same conditions and comparing their means. In plants the two groups are often the progeny of self-pollination and of cross-pollination.[3] The result is written δ, the shortfall of the inbred group as a proportion of the outbred value: (woutbred − winbred) / woutbred. A δ of 0 means no difference. A δ of 0.5 means that the inbred group reaches half the outbred value.[9]
Fitness itself can be measured only in certain laboratory populations of Drosophila, Escherichia coli and yeast. Most data therefore concern components of fitness such as viability, female fecundity or male mating success.[3] Surveys of plants divide the life cycle into seed production, germination, juvenile survival and growth and reproduction. They add a cumulative value for the whole cycle.[4][10] A loss at one stage can be offset at a later one through reduced competition among the survivors, so Armbruster and Reed favour composite measures that cover as much of lifetime reproductive success as possible.[1]
Experiments at different levels of inbreeding are compared through the inbreeding load, B. It is the slope of the natural logarithm of a trait's mean against the inbreeding coefficient F: ln zoutbred − ln zinbred = BF. B is the fall in log fitness that complete inbreeding would bring. It is counted in lethal equivalents and is zero when there is no depression.[3][1] A 2006 review of vertebrates by O'Grady and colleagues found a total of about six lethal equivalents per haploid genome, about two in fecundity and four in survival.[11]
These calculations assume that allele frequencies do not change during inbreeding.[3] Where a trait goes with fitness, natural selection during inbreeding is likely to leave the mean above the predicted value.[12] A further explanation of a gap between selfed and outcrossed progeny is that a varied set of plants uses resources better than a uniform one, an idea with little direct support from plant experiments.[3]
Partial dominance and overdominance
At a single locus with allele frequency p and genotype fitnesses wAA, wAa and waa, an inbreeding coefficient f lowers mean fitness by f p(1 − p)(2wAa − wAA − waa). The mean falls whenever the heterozygote lies above the average of the two homozygotes. That holds for an overdominant locus, for a locus where the fitter allele is dominant and even for slight partial dominance of the fitter allele. A rare recessive allele is affected most: at p = 0.001 its homozygotes rise from one in a million to one in a thousand as f goes from 0 to 1.[13]
Under the dominance hypothesis the cause is recessive or partially recessive deleterious alleles, held in the population by recurrent mutation or by balancing selection. Under the overdominance hypothesis it is loci with heterozygote advantage, whose alleles stay polymorphic.[3] E.M. East held the second view for yield in maize and D.F. Jones the first. Neither can be told from the other by examining the mean.[12]
In Drosophila melanogaster, lethal second chromosomes lower viability by only 2 to 3 per cent on average when heterozygous. Estimates of the mean dominance coefficient, which pure overdominance predicts to be zero, run from about 0.12 for viability to above 0.26 for most other fitness components. Sperm precedence is the exception. The lethal part of the load, about half of the total for viability, is mutational in origin. On the mutation rates then available, mutation appeared to explain only about 60 per cent of the rest of the load for fitness components and 30 per cent for net fitness. That leaves room for alleles kept by balancing selection with antagonistic pleiotropy.[3]
Overdominance estimated in the F2 of a cross between inbred lines tends to shrink after further generations of recombination, in maize and in other plants. Partially recessive alleles linked to a marker can make the marker's heterozygotes look superior, which is called associative overdominance or pseudo-overdominance.[3] Charlesworth and Charlesworth concluded in 1999 that depression in most fitness components probably reflects partial recessivity. A 2009 review by Deborah Charlesworth and John Willis found it predominantly caused by recessive deleterious mutations.[3][2] In a partial diallel of maize hybrids, most putatively deleterious SNPs showed incomplete dominance. The more damaging variants tended to be more recessive. The authors expected overdominance to contribute too.[14]
García-de Heer and colleagues name both mechanisms for cannabis and write that their relative impact varies among species and populations.[5] Mishchenko and colleagues write that the models do not fully explain inbreeding depression, citing reports of epigenetic changes in inbred maize.[7]
Purging and the mating system
Homozygotes for deleterious alleles are more frequent in an inbred population, so selection acts on those alleles more effectively than under random mating.[3] Alleles of major effect are readily purged. Alleles with small selection coefficients may be almost impossible to purge without selection between lines.[3] Inbreeding cannot purge an overdominant locus.[11] Genetic drift acts at the same time: the chance fixation or loss of deleterious alleles lowers the inbreeding load without purging and can leave mean performance no better. Purging is better detected by comparing inbred genotypes from the population in question with genotypes of similar inbreeding coefficient from an outbred one.[3]
Crnokrak and Barrett collated 28 experimental studies, covering 13 plant species among other organisms. They found frequent and substantial purging by each of three measures. The measures agreed poorly within individual studies, and the authors allow that rebounds in fitness may partly reflect adaptation to laboratory conditions.[15] In the outcrossing Mimulus guttatus, five generations of selfing single plants, during which a high proportion of lines failed, reduced inbreeding depression only slightly.[3]
Husband and Schemske compiled estimates for 79 populations of 54 vascular plant species. Mean δ was 0.23 in predominantly selfing species and 0.53 in predominantly outcrossing ones. The gap lay in seed production (0.05 against 0.32), germination (0.02 against 0.12) and survival to reproduction (0.04 against 0.15). There was no gap in growth and reproduction (0.21 against 0.27). They took early-acting depression to come mostly from recessive lethals that inbreeding can purge. Late-acting depression they put mostly down to weakly deleterious mutations that are very hard to purge.[4] The lower load of selfing species could also come from their failure to keep variation at overdominant loci.[3] Across 58 species, Winn and colleagues found mean lifetime δ of 0.58 in mixed-mating populations and 0.54 in highly outcrossing ones, which they judged inconsistent with most mixed-mating taxa evolving towards selfing.[10]
Stress and small populations
Armbruster and Reed reviewed 34 studies that measured inbreeding depression in more than one environment, a stressful environment being one that lowers fitness relative to another. Depression was greater under stress in 76 per cent of cases, though significantly so in only 48 per cent. Mean B was 1.45 lethal equivalents under stress and 0.85 under benign conditions. Lineages within a species often responded differently.[1] Inbreeding generally raises a population's sensitivity to stress, which adds to the effects of genetic erosion on small populations facing pollution or climate change.[9]
Across 116 studies of 107 plant species, inbreeding depression increased with population size, a pattern that may reflect a higher baseline of inbreeding or more purging in small populations.[16] In a small population, inbreeding depression, drift and chance events can feed one another in a decline called the extinction vortex. Purging helps only a population with enough diversity to survive the first rise in depression.[17] Simulations by Caballero and colleagues, with a load of six lethal equivalents, put the minimum effective population size for keeping the fall in fitness below 10 per cent over five generations at about 70. Calculations that ignore purging give more than 142. The same study found that circular mating of siblings, tried as a way of forcing purging, carried too high a risk of extinction at such loads to be advised in captive breeding.[11]
Genetic rescue brings gene flow into an inbred population. In a meta-analysis of 156 cases judged at low risk of outbreeding depression, Frankham found benefits in 92.9 per cent, with a median rise in composite fitness of 148 per cent in stressful environments and 45 per cent in benign ones.[18] Outbreeding depression is the opposite risk, when populations with different local adaptations are mixed.[19] The plant numbers set for regrowing cannabis accessions are described under effective population size.
What is measured in cannabis
Measurements in cannabis are of single characters in selfed progeny, set against outcrossed progeny, the starting plants or the original accession. All of them come from cultivars, breeding lines and landrace accessions under cultivation.
| Plants | Selfed generation | Compared with | Result |
|---|---|---|---|
| Hemp strain Candida (CD-1), feminised | First | Outcrossed progeny of two crosses | Half the height and total dry weight; floral dry weight 63 per cent lower[6] |
| Two families from a hemp cultivar, in a trial of 23 families | Second | Other families | Growth of 1.46 and 1.03 cm a day, against 2.75 in the fastest family[20] |
| Monoecious hemp Hlukhivski 58 | First, fourth to sixth, twelfth | Starting plants | Seed mass per plant 11.3, 50.9–52.2 and 74.9 per cent lower[7] |
| Monoecious hemp Zolotoniski 15 | First, twelfth | Starting plants | Seed mass per plant 20.6 and 50.3 per cent lower[7] |
| Monoecious hemp Hlesiia | First, twelfth | Starting plants | Seed mass per plant 16.9 and 65.0 per cent lower[7] |
| Hang Kra Rok landrace, two accessions | First | F1 between the accessions | No difference in dry flower weight; height of 78.94 and 74.83 cm, against 87.22 and 88.78 cm[8] |
| Four accessions | Sixth | Original accessions | Total dry weight lower in two, no different in two[5] |
Germination and survival
Field germination of self-pollinated hemp lines at Penza in Russia ranged from 0 to 67 per cent in the first selfed generation and from 0 to 47 per cent in the second. Low germination, which Serkov and Klimova put down to inbreeding depression, limited how many lines could be grown. Later ranges were 0 to 59, 10 to 85 and 0 to 100 per cent. Between one and six lines dropped out in each generation. Germination tended to rise in the later generations. The authors attribute germination and survival both to the weather of the year and to the degree of depression.[21]
Size and yield
In Hlukhivski 58 every main character had shifted by the first selfed generation, stem and fibre mass by more than 10 per cent. By the twelfth generation stem mass was 47.0 per cent lower, fibre mass 55.0 per cent and seed mass per plant 74.9 per cent. The southern cultivar Zolotoniski 15 tended to lose less. The authors write that depression went deepest in the character each cultivar expressed most strongly: stem and fibre mass in Zolotoniski 15, seed mass in Hlesiia, a cultivar grown mainly for seed. Not every character fell: technical stem length rose in the later generations of Hlukhivski 58 and the thousand-seed weight of Zolotoniski 15 rose in the first. The authors tie the depression in yield to a smaller leaf area.[7] In earlier Soviet work R.I. Kaplunova reported a sharp drop in productivity, of 25 to 30 per cent, in the first generation.[21]
The Candida progeny in the table all had variegated leaves, a recessive trait in higher plants that their parent did not show. They flowered seven days later than the outcrossed plants.[6] The selfed Hang Kra Rok plants flowered about a week earlier than the F1 plants. Srikul and colleagues, growing the plants in a plant factory under artificial light, found no inbreeding depression in flower yield and suggested that deleterious alleles might have been purged in the landrace's past.[8] García-de Heer and colleagues kept the most vigorous seedling of each generation. They write that this selection may partly account for the two lines that did not lose dry weight.[5]
Abnormal plants and flowers
Mishchenko found 18 kinds of abnormal plant in the first two selfed generations of two Ukrainian cultivars, among them dead growing tips, forked inflorescences, fasciated stems, male and female sterility and dwarfism. In Hlukhivski 58 they made up 5.43 per cent of first-generation plants and 3.14 per cent of the second, against 2.15 per cent in the cultivar itself. In Zolotoniski 15 the shares were 3.96, 2.26 and 0.76 per cent. The author could not say which were mutations and which were non-heritable changes.[22]
From the fourth generation of selfing, every line of García-de Heer and colleagues produced abnormal flowers and set less seed. Grown side by side, the seven generations of one line rose from 0.4 per cent abnormal flowers in the starting plants to 13.7 per cent in the sixth selfed generation. Treating different parts of a plant with both silver thiosulfate and ethephon restored seed set. The authors took this to indicate that inbreeding depression was affecting hormone signalling, perhaps that of ethylene.[5] Pollen supply in these lines is described under inbred line.
Over successive generations
In all three Ukrainian cultivars the characters settled in the fourth to sixth generations, at what the authors call the inbred minimum. They link the further fall by the twelfth generation in Hlukhivski 58 chiefly to a change in the sexual make-up of the lines: from the sixth generation most offspring were monoecious plants with mostly male flowers and fewer lines could give viable offspring.[7] In the dwarf autoflowering cultivar Wilhelmina, selfed for four generations, means did not change while variation within lines fell. The fourth-generation plants were uniformly small. Infertile plants with yellow, malformed leaves and a severely dwarfed habit made up 40 per cent of the first and second generations, 10 per cent of the third and none of the fourth. McDonald and Lubell-Brand suggested that the trait might have been eliminated and called for more seedlings to be grown to confirm it.[23]
Each generation at Penza was grown in its own year, from 2007 to 2011. Mean seed yield per plant was 13.6 grams in the first, 1.1 grams in the fourth and 22.7 grams in the fifth. The authors put the low values of the fourth generation mostly down to an extremely dry season.[21]
García-de Heer and colleagues found the effect variable across their lines and concluded that homozygosity can be reached without severe harm in at least some cultivars, given selection for vigour in each generation. They also judged inbred lines unlikely to suit commercial production themselves.[5]
See also
References
- ↑ 1.0 1.1 1.2 1.3 Armbruster, P.; Reed, D.H. (2005). "Inbreeding depression in benign and stressful environments". Heredity. 95 (3): 235–242. doi:10.1038/sj.hdy.6800721.
- ↑ 2.0 2.1 Charlesworth, D.; Willis, J.H. (2009). "The genetics of inbreeding depression". Nature Reviews Genetics. 10 (11): 783–796. doi:10.1038/nrg2664.
- ↑ 3.00 3.01 3.02 3.03 3.04 3.05 3.06 3.07 3.08 3.09 3.10 3.11 3.12 3.13 3.14 3.15 Charlesworth, B.; Charlesworth, D. (1999). "The genetic basis of inbreeding depression". Genetical Research. 74 (3): 329–340. doi:10.1017/S0016672399004152.
- ↑ 4.0 4.1 4.2 Husband, B.C.; Schemske, D.W. (1996). "Evolution of the magnitude and timing of inbreeding depression in plants". Evolution. 50 (1): 54–70. doi:10.1111/j.1558-5646.1996.tb04472.x.
- ↑ 5.0 5.1 5.2 5.3 5.4 5.5 5.6 Garcia-de Heer, L.; Mieog, J.; Burn, A.; Nolan, M.; Liu, L.; et al. (2026). "Weeding out variability: a proof-of-concept for producing uniform F1 hybrid Cannabis sativa L. using single-seed descent". Horticulture Research. 13 (5) uhag038. doi:10.1093/hr/uhag038. PMC 13188225.
- ↑ 6.0 6.1 6.2 Kurtz, L.E.; Mahoney, J.D.; Brand, M.H.; Lubell-Brand, J.D. (2020). "Comparing genotypic and phenotypic variation of selfed and outcrossed progeny of hemp". HortScience. 55 (8): 1206–1209. doi:10.21273/HORTSCI15061-20.
- ↑ 7.0 7.1 7.2 7.3 7.4 7.5 7.6 7.7 Міщенко, С.В.; Кабанець, В.М.; Кириченко, Г.І.; Марченко, Т.Ю.; Мачульський, Г.М. (2025). "Особливості прояву ознак однодомних конопель в процесі інбридингу та його використання в селекції" [Features of the expression of the traits of monoecious hemp in the inbreeding process and its use in breeding]. Faktori eksperimental'noi evolucii organizmiv (in українська). 37: 29–34. doi:10.7124/FEEO.v37.1742.
- ↑ 8.0 8.1 8.2 Srikul, Pichsiri; Mayong, Amonrat; Matthayatthaworn, Weerachai; Sreewongchai, Tanee (2026). "Comparison of self-pollination and intercrossing for feminized seed production in Thai Hang Kra Rok cannabis (Cannabis sativa L.) landrace". Agriculture and Natural Resources. 60 (5) 600512. doi:10.34044/j.anres.2026.60.5.12.
- ↑ 9.0 9.1 Bijlsma, R.; Loeschcke, V. (2012). "Genetic erosion impedes adaptive responses to stressful environments". Evolutionary Applications. 5 (2): 117–129. doi:10.1111/j.1752-4571.2011.00214.x. PMC 3353342.
- ↑ 10.0 10.1 Winn, A.A.; Elle, E.; Kalisz, S.; Cheptou, P.-O.; Eckert, C.G.; et al. (2011). "Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating". Evolution. 65 (12): 3339–3359. doi:10.1111/j.1558-5646.2011.01462.x.
- ↑ 11.0 11.1 11.2 Caballero, A.; Bravo, I.; Wang, J. (2017). "Inbreeding load and purging: implications for the short-term survival and the conservation management of small populations". Heredity. 118 (2): 177–185. doi:10.1038/hdy.2016.80. PMC 5234482.
- ↑ 12.0 12.1 Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. pp. 411–414.
- ↑ Felsenstein, J. (December 2019). Theoretical evolutionary genetics. Seattle: Department of Genome Sciences, University of Washington. pp. 242–244.
- ↑ Yang, J.; Mezmouk, S.; Baumgarten, A.; Buckler, E.S.; Guill, K.E.; et al. (2017). "Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize". PLOS Genetics. 13 (9) e1007019. doi:10.1371/journal.pgen.1007019. PMC 5633198.
- ↑ Crnokrak, P.; Barrett, S.C.H. (2002). "Perspective: purging the genetic load: a review of the experimental evidence". Evolution. 56 (12): 2347–2358. doi:10.1111/j.0014-3820.2002.tb00160.x.
- ↑ Angeloni, F.; Ouborg, N.J.; Leimu, R. (2011). "Meta-analysis on the association of population size and life history with inbreeding depression in plants". Biological Conservation. 144 (1): 35–43. doi:10.1016/j.biocon.2010.08.016.
- ↑ Davinack, D. (2024). Molecular Ecology & Evolution: An Introduction. Norton, Massachusetts: Wheaton College. pp. 172–174.
- ↑ Frankham, R. (2015). "Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow". Molecular Ecology. 24 (11): 2610–2618. doi:10.1111/mec.13139.
- ↑ Davinack, D. (2024). Molecular Ecology & Evolution: An Introduction. Norton, Massachusetts: Wheaton College. pp. 182–183.
- ↑ Carlson, C.H.; Stack, G.M.; Jiang, Y.; Taşkıran, B.; Cala, A.R.; et al. (2021). "Morphometric relationships and their contribution to biomass and cannabinoid yield in hybrids of hemp (Cannabis sativa)". Journal of Experimental Botany. 72 (22): 7694–7709. doi:10.1093/jxb/erab346.
- ↑ 21.0 21.1 21.2 Serkov, V.A.; Klimova, L.V. (2016). "Sozdanie i izuchenie samoopylennykh linii dlya prakticheskoi selektsii nenarkoticheskoi konopli posevnoi" [Creation and study of self-pollinated lines for the practical breeding of non-narcotic seed hemp]. Niva Povolzh'ya (in русский) (2 (39)): 52–60.
- ↑ Міщенко, С.В. (2011). "Зміна ознак рослин конопель у потомстві самозапилених особин сортів середньоросійського і південного типів" [Change of traits of hemp plants in the progeny of self-pollinated individuals of Central-Russian and southern-type cultivars]. Plant Breeding and Seed Production (in українська) (100): 120–130. doi:10.30835/2413-7510.2011.66536.
- ↑ McDonald, M.M.; Lubell-Brand, J.D. (2024). "F1 hybrid seed can enhance cannabis crop uniformity and yield". HortScience. 59 (12): 1795–1799. doi:10.21273/HORTSCI18197-24.