Conservation genetics
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Conservation genetics applies genetics to the conservation of species and populations. Its central idea is that small, isolated populations face genetic threats besides demographic ones. In a population of few individuals, genetic drift and inbreeding dominate how variation changes. Drift loses and fixes alleles at random, so that favourable alleles can be lost and harmful ones fixed, while inbreeding raises the frequency of homozygotes.[1] The field usually measures genetic diversity as neutral variation across the genome and uses it to judge the health of populations and their risk of extinction.[2]
The field rested mainly on theory until markers based on the polymerase chain reaction, such as microsatellites, became easy to apply. Studies could then test whether small populations hold less variation and are more inbred. A search of the Web of Science for papers naming the field and a type of marker found four in 1990 and 682 in 2009.[1] Genomic methods have since made it possible to estimate variation across whole genomes, including variation that affects fitness.[1] In 2021 two groups of authors disagreed over whether conservation should go on giving priority to variation across the genome or turn to the functional variation thought to affect fitness.[2][3]
The Convention on Biological Diversity of 1992 recognises three levels of biodiversity: diversity within species, between species and of ecosystems. Its targets and indicators for genetic diversity long dealt mainly with agricultural species and their wild relatives.[4] For crops, the concerns of the field meet the work of gene banks and of ex situ and in situ conservation. In Cannabis, regrowing stored seed may lose variation by drift.[5] Feral populations in the United States have been genotyped to stock a gene bank.[6]
Small populations
In a closed population that mates at random, heterozygosity falls in each generation by a fraction set by the effective population size, Ne. After t generations, Ht/H0 = (1 − 1/2Ne)t = 1 − F, where F is the inbreeding coefficient. Small, closed populations that reproduce sexually therefore cannot avoid inbreeding and loss of variation. Inbreeding and loss of variation build up from one generation to the next. In wild populations the effective size averages a tenth to a fifth of the census size, the number of adults counted.[7]
Small size has three genetic consequences. Homozygosity rises and harmful alleles become commoner, which often brings inbreeding depression (a fall in the average fitness of individuals) and may lower the viability of a population in the short term. The loss of variants reduces the population's capacity to adapt and so its viability in the long term, above all where the environment changes. Small, isolated populations also drift apart from one another. Crossing them later, for example to restore gene flow, may then bring outbreeding depression.[1]
A population bottleneck has these effects quickly. In simulated populations that fall sharply in number, nucleotide diversity declines over the following generations. The harmful alleles that remain often rise to high frequency or to fixation. Drift load, the loss of mean fitness caused by homozygosity for harmful alleles, can therefore become high before diversity has fallen far.[3]
Species are usually driven to extinction by threats from human activity, among them habitat loss, over-exploitation, introduced species, pollution and climate change, together with chance events that weigh on small populations: demographic, environmental and genetic stochasticity and catastrophes. These typically reinforce one another in a feedback called the extinction vortex.[7]
Genetics and extinction
Whether genetic factors contribute to extinction has been disputed. Russell Lande argued in 1988 that demography may usually be of more immediate importance than population genetics in setting the minimum viable size of wild populations. Derek Spielman, Barry Brook and Richard Frankham write that the argument was widely interpreted to mean that ecological and demographic causes drive threatened populations to extinction before genetic ones have time to act.[8]
In 2004 Spielman and colleagues compared the average heterozygosity of 170 threatened taxa with that of related taxa not under threat. Heterozygosity was lower in the threatened taxon in 77 per cent of comparisons, by 35 per cent on average and 40 per cent at the median. Among the 36 plant taxa, 75 per cent had lower heterozygosity than their relatives. The authors concluded that most taxa are not driven to extinction before genetic factors affect them. They could not determine whether genetic factors had contributed to the threatened status of the taxa they studied. In computer projections for 20 threatened species that they cite, adding inbreeding depression in juvenile survival shortened the median time to extinction by 24 to 31 per cent.[8]
In field populations of the Glanville fritillary butterfly, the level of inbreeding in a population was correlated with its probability of extinction. Inbred laboratory lines of Drosophila melanogaster went extinct at higher rates than lines that were not inbred, most clearly under stressful conditions. Joop Ouborg and colleagues still judged in 2010 that how far inbreeding depression affects the persistence of populations and species was an open question, beyond a few well-studied examples.[1] In the plant Clarkia pulchella, an increase of 5 per cent in the inbreeding coefficient raised the share of populations going extinct from 25 to 69 per cent.[7]
Population viability analyses, computer models that estimate a population's chance of persisting, have often left genetics out. In the decade before 2014 many analyses still left genetic factors out. Most of those that did applied 3.14 lethal equivalents of inbreeding depression to juvenile survival, the default setting of the Vortex software, while the average for total fitness in the wild is about 12. A lethal equivalent is a set of harmful alleles that would on average cause death if homozygous.[7][3]
How large a population must be
In 1980 Franklin and Soulé proposed that an effective size of 50 would prevent inbreeding depression in the short term. The figure rested on the opinion of animal breeders and on limited data from domestic and laboratory animals. Franklin put the size needed to keep the capacity to evolve indefinitely at 500, from the balance between the additive variation that mutation supplies and the variation that drift removes. The resulting 50/500 rule shaped the population-size thresholds of criterion C of the IUCN Red List.[7]
Frankham, Corey Bradshaw and Barry Brook argued in 2014 that both figures should be at least doubled. They estimated that five generations at an effective size of 50 would cost a wild population 26 per cent of its total fitness. They proposed an effective size of at least 100 to hold the loss below 10 per cent over five generations and at least 1,000 to keep the capacity to evolve. The Red List thresholds of criterion C, they argued, should be doubled to match, for example from fewer than 250 to fewer than 500 for a critically endangered taxon.[7]
A minimum viable population is the size a population needs to persist with high probability over the long term. It has been estimated for few species. Frankham and colleagues proposed a common standard, the size giving a 99 per cent chance of persisting for 40 generations, which for a typical outbreeding species is of the order of several thousand.[7]
In 2020 Sean Hoban and 30 co-authors proposed an indicator for the Convention on Biological Diversity: the number of populations within species with an effective size above 500 against the number below it. Where no estimate exists, they suggested taking a tenth of the census size, so that a population of 5,000 adults is taken to have an effective size of about 500. In their view an effective size below 50 calls for immediate action.[4]
Neutral and functional variation
Studies with neutral markers such as microsatellites and amplified fragment length polymorphisms tested whether population size predicts variation and inbreeding. They also estimated gene flow, effective size and population history and helped define evolutionarily significant units. Meta-analyses of plant and animal studies found that smaller populations hold less genetic variation and have lower average fitness. The link with fitness is thought to be largely genetic but is also affected by non-genetic processes tied to population size, such as the Allee effect and the decline of local habitat.[1]
Neutral markers cannot measure variation under selection directly. Studies typically used 10 to 20 of them. Ouborg and colleagues set out four questions this left open: whether small size erodes variation that affects fitness as it erodes neutral variation, how variation is linked to fitness and adaptation, how genetic and environmental effects interact and how drift and inbreeding change the activity of genes. They expected genome-wide single-nucleotide polymorphisms, genome scans that separate neutral from selected loci and studies of gene expression to answer them.[1]
João Teixeira and Christian Huber argued in 2021 that neutral genetic diversity has only very limited relevance for conservation. They pointed to the weak relation between a species' Red List status and its genome-wide nucleotide diversity. They named species with almost no variation and no observed loss of fitness, among them the San Nicolas island fox, the vaquita and the brown hyena. They also cited studies finding that species low in diversity do not accumulate adaptive substitutions at a much lower rate. They called for mapping the variation that affects fitness and adaptation. In their view the best way to preserve biodiversity is to restore and conserve natural ecosystems.[2]
Marty Kardos and seven co-authors replied that theory and empirical results show conserving genome-wide variation to be generally the best way to keep inbreeding depression and lost adaptive potential from driving populations to extinction. Small populations with little variation lose some harmful alleles through drift and purging, but they are still expected to have lower mean fitness. Red List status is a subjective index of extinction risk. A population also loses its variation only some generations after it declines. The simulations recently used to discount genome-wide variation, Teixeira and Huber's among them, assumed rates of harmful mutation 2.6 to 92.3 times lower than the best estimate for Drosophila. Managing a few chosen loci, Kardos and colleagues argued, risks the loss of variation elsewhere in the genome.[3]
Gene flow and genetic rescue
Fragmentation splits species into populations that exchange few migrants. Frankham and colleagues judged it a serious genetic threat. In more than a quarter of species, populations differ markedly, with a fixation index (FST) above 0.2. Within species, genetic diversity and mean fitness typically rise with population size. For populations once connected that have lost gene flow and show genetic erosion, they recommended considering an increase in gene flow where the risk of outbreeding depression is low.[7]
Crossing a small, inbred population with another to restore its fitness is called genetic rescue. By 2018 only about 30 genetic rescues of wild plant and animal populations had been attempted for conservation, the Florida panther among them. Inbreeding was mentioned in only 7 per cent of recovery plans for endangered species in the United States, Australia and Europe. A meta-analysis of 156 data sets by Frankham in 2015 found that outcrossing benefited inbred populations in 93 per cent of cases.[9] Katherine Ralls and seven co-authors hold that fears of outbreeding depression are exaggerated: it is uncommon, often transient and usually smaller in effect than inbreeding depression. The risk of a particular cross can be assessed with a published decision tree.[9]
Ralls and colleagues proposed that where the risk of outbreeding depression is low, the default should be to evaluate restoring gene flow to small, inbred populations of diploid outbreeding species that human activity isolated within the last 500 years. A population with an inbreeding coefficient of 0.1, or one that has lost 10 per cent of its genetic diversity, should be assumed to need management. They separate differences between populations that come from drift, where genetic rescue should be considered, from differences that reflect adaptation to different environments, which usually call for separate management. To choose a source population they recommend minimising mean kinship. FST can mislead, since it is often highest against inbred populations, which are poor sources.[9]
Ouborg and colleagues note that strong local adaptation would call for managing populations one by one, not for promoting dispersal among them.[1] Crossing can also break up combinations of genes adapted together. The resulting fall in fitness may appear only after the first two hybrid generations, which experiments seldom follow.[2] On Isle Royale, a single immigrant male wolf at first raised reproduction in a small population, then caused very high inbreeding within two generations, after which the population declined sharply. Kardos and colleagues consider the case unusual, since managed rescues usually move several individuals.[3]
Crops and genetic resources
Genetic erosion has two common meanings. In the conservation literature it usually means the loss of alleles, of heterozygosity, of distinct populations or of gene flow. In the agricultural literature it more often means the loss of varieties, landraces, breeds or traits. Hoban and colleagues proposed one definition for both. In their view endangered breeds of domestic species are comparable to endangered distinct wild populations. Populations, they write, are the wild equivalent of breeds or plant varieties.[4]
The Convention on Biological Diversity's target on genetic diversity for 2011 to 2020 named cultivated plants, farmed and domesticated animals and their wild relatives. The first draft of its framework for after 2020 again proposed counting the plant genetic resources for food and agriculture held in medium- or long-term storage, in practice the number of seed accessions. Hoban and colleagues judge this count only loosely connected to genetic diversity, since a seed bank often holds the offspring of a single population or of a few individuals. They proposed counting collections that are representative, sampled across the range and typically from at least five populations; resilient, with seed from more than 50 plants per population; and replicated in more than one place.[4] How many plants and populations to sample is the subject of germplasm sampling.
Stored seed has to be regrown from time to time. Each regrowing is a small population. Genetic drift during regeneration has reduced the variation held in gene bank collections of barley, maize and common bean. Much of the loss depends on the number of parents used. A core collection, a subset chosen to cover the range of a species' diversity with as little repetition as possible, allows the gene pool to be characterised and used more efficiently.[5]
In cannabis
Cannabis is mostly dioecious and outbreeding. Few if any intact wild populations are thought to exist. Its gene pool is thought to consist mainly of domesticated and feral populations, cultivars and selections. Matthew Welling and colleagues reviewed the plant's stored germplasm in 2016. Of 808 accessions they found reported from collections worldwide, 58 (7.2 per cent) came from China. Citing the long cultivation of the plant in East Asia, its apparently high diversity there and its scarcity in published collections, they judged East Asian germplasm a priority for conservation. They call the regrowing of cannabis accessions especially problematic. The plant is wind-pollinated, so outdoor plots may need to stand up to 5 km apart. Pollen-proof indoor facilities limit how many plants can be crossed, so allelic variation may decline with each regrowing. They suggested that cryopreservation of seed could reduce the hybridisation and drift that regrowing brings. The markers used so far to survey cannabis diversity, they noted, may not reflect functional variation or the population structure that conservation needs.[5]
Welling and colleagues proposed an international core collection of up to 400 accessions drawn from existing gene banks, which on theoretical grounds should hold 99 per cent of the alleles that occur at species-wide frequencies above 2 per cent. Limits on moving seed between countries party to the Single Convention on Narcotic Drugs and the Convention on Psychotropic Substances led them to propose a virtual collection instead, built from shared data. They concluded that the international drug conventions had, over more than 50 years, been "influential in the fractionation and erosion" of publicly accessible collections.[5]
Ademola Aina and colleagues collected seed from 1,815 female plants in 88 feral populations across 12 states of the United States in 2022 and 2023, to stock the hemp collection of the National Plant Germplasm System. They genotyped 760 plants. The 346 plants that could be assigned firmly to a group fell into five genetic groups that largely followed their state of origin, with FST between groups of 0.07 to 0.39. Observed heterozygosity across these plants, 0.20, matched the expected value, which the authors read to mean that the populations were not markedly inbred. A north-eastern group of 14 plants had an observed heterozygosity of 0.09, less than half that of the others. The authors suggest that this may come from its small population size and geographic isolation.[6]
See also
References
- ↑ 1.0 1.1 1.2 1.3 1.4 1.5 1.6 1.7 Ouborg, N.J.; Pertoldi, C.; Loeschcke, V.; Bijlsma, R.; Hedrick, P.W. (2010). "Conservation genetics in transition to conservation genomics". Trends in Genetics. 26 (4): 177–187. doi:10.1016/j.tig.2010.01.001.
- ↑ 2.0 2.1 2.2 2.3 Teixeira, J.C.; Huber, C.D. (2021). "The inflated significance of neutral genetic diversity in conservation genetics". Proceedings of the National Academy of Sciences. 118 (10) e2015096118. doi:10.1073/pnas.2015096118. PMC 7958437.
- ↑ 3.0 3.1 3.2 3.3 3.4 Kardos, M.; Armstrong, E.E.; Fitzpatrick, S.W.; Hauser, S.; Hedrick, P.W.; Miller, J.M.; Tallmon, D.A.; Funk, W.C. (2021). "The crucial role of genome-wide genetic variation in conservation". Proceedings of the National Academy of Sciences. 118 (48) e2104642118. doi:10.1073/pnas.2104642118. PMC 8640931.
- ↑ 4.0 4.1 4.2 4.3 Hoban, S.; Bruford, M.; D'Urban Jackson, J.; Lopes-Fernandes, M.; Heuertz, M.; et al. (2020). "Genetic diversity targets and indicators in the CBD post-2020 Global Biodiversity Framework must be improved". Biological Conservation. 248 108654. doi:10.1016/j.biocon.2020.108654.
- ↑ 5.0 5.1 5.2 5.3 Welling, M.T.; Shapter, T.; Rose, T.J.; Liu, L.; Stanger, R.; King, G.J. (2016). "A belated green revolution for Cannabis: virtual genetic resources to fast-track cultivar development". Frontiers in Plant Science. 7 1113. doi:10.3389/fpls.2016.01113.
- ↑ 6.0 6.1 Aina, Ademola; Wenger, Jonathan P.; Stanton, Eliot; Majumdar, Chandrani Gon; ElSohly, Mahmoud; Weiblen, George D.; Ellison, Shelby (1 July 2025). "Genetic diversity, population structure, and cannabinoid variation in feral Cannabis sativa germplasm from the United States". Scientific Reports. 15 (1) 20423. doi:10.1038/s41598-025-07912-8. PMC 12215616.
- ↑ 7.0 7.1 7.2 7.3 7.4 7.5 7.6 7.7 Frankham, R.; Bradshaw, C.J.A.; Brook, B.W. (2014). "Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses". Biological Conservation. 170: 56–63. doi:10.1016/j.biocon.2013.12.036.
- ↑ 8.0 8.1 Spielman, D.; Brook, B.W.; Frankham, R. (2004). "Most species are not driven to extinction before genetic factors impact them". Proceedings of the National Academy of Sciences. 101 (42): 15261–15264. doi:10.1073/pnas.0403809101. PMC 524053.
- ↑ 9.0 9.1 9.2 Ralls, K.; Ballou, J.D.; Dudash, M.R.; Eldridge, M.D.B.; Fenster, C.B.; Lacy, R.C.; Sunnucks, P.; Frankham, R. (2018). "Call for a paradigm shift in the genetic management of fragmented populations". Conservation Letters. 11 (2) e12412. doi:10.1111/conl.12412.