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Genetic diversity and resilience in benthic marine populations

Revista Chilena de Historia Natural volume 96, Article number: 4 (2023) Cite this article

Abstract

Background

Understanding the mechanisms behind resilience has become more relevant in the last decades, due to the increasing and intensifying disturbances from natural and anthropogenic sources that threaten biodiversity. Evidence from terrestrial populations suggests that resilience increases with genetic diversity. Few studies, however, have evaluated the relationship between genetics and resilience in benthic marine populations.

Methods and results

For this review, we gathered studies where genetic diversity was the predictor variable, and resilience was the response variable. Twenty-five publications between 2001 and 2018 were included. Thirteen benthic marine species were identified, mainly sea-grass species, among which Zostera marina was the most frequently studied. The relationship between genetic diversity and resilience was variable-dependent. Considering all the analyses (N = 150) in the studies reviewed, 44% reported positive relationships between genetic diversity and resilience capacity. Negative relationships were found in 6%, and no relationship was found in 50%. Positive relationships indicated that genetic diversity increased resistance and recovery capacity after different types of disturbances. Dominance and complementarity were suggested as the underlying mechanism explaining these findings in the few studies that conducted this type of evaluation.

Conclusions

The results of this review suggest that the relationship between genetic diversity and resilience is mainly positive. However, this relationship relies on how genetic diversity and resiliency were measured, as well as on the biological characteristics of the species under study. This reinforces the importance of acknowledging and maintaining genetic diversity for the conservation of benthic populations in marine ecosystems.

Background

Given that the frequency and intensity of disturbances are increasing in marine ecosystems due to anthropogenic activity and climate change, it is important to evaluate underlying mechanisms that increase population resilience capacity [1, 2]. There is supporting evidence for the hypothesis that greater genetic diversity in natural populations would maximize resistance and adaptive potency when facing biotic and abiotic environmental changes. However, recent studies have demonstrated that populations may be able to adapt by means of a few large-effect variants despite low overall genetic diversity [3]. Accordingly, questions have arisen regarding the importance of neutral genetic diversity versus functional genetic diversity [4].

Genetic diversity has important consequences, to which all organizational levels of biodiversity are connected. It affects individual biological fitness, population viability, adaptability of species to environmental changes, evolutionary potential, as well as the structure and functioning of communities and ecosystems, particularly during periods of environmental stress, providing higher resilience capacity [5,6,7]. At the individual level, heterozygosity has been positively related to fitness (heterosis), and is associated with higher adaptive phenotype plasticity [8,9,10,11,12]. Genetic variation among individuals within a population provides a base mechanism for plasticity and adaptability. This allows for a greater range of possible functional responses (physiological versatility), occupying different niches, promoting population diversity, and hence, higher resilience under environmental stress or disturbances [5, 7].

Genetic variation among populations and subpopulations may be evaluated based on degrees of relatedness among individuals. Greater endogamy increases homozygosity in the genome and can decrease biological fitness by inbreeding depression and the expression of lethal recessive alleles. On the contrary, extreme exogamy may diminish biological fitness due to heterozygote disadvantage, and the breaking up of complex co-adapted advantageous genes, or because of low adaptation [13].

Under a regime of frequent and expectable disturbances, some organisms, through their evolutionary history and selective processes, have been able to develop local adaptations that reduce the risk of mortality and maximize fitness in temporally unstable environments [14, 15]. However, the capacity to develop adaptations and survive extreme conditions becomes difficult when the frequency and severity of natural and anthropogenic disturbances escalate.

Several studies have evaluated population resilience (e.g., [1, 7]). However, the concept of resilience is quite controversial, given that it involves many definitions that have accumulated over time, producing confusion and the synonymous or complementary use of terms such as persistence, resistance, recovery, and stability. The word resilience was coined by Elton in 1958. He defined it as “the possibility for communities to resist some disturbance and not suffer structural changes” [16]. In 1973, Holling defined resilience as “the measure of the persistence of systems and their capacity to absorb changes and disturbances, keeping the same relations between populations or variable states” [17]. Later in 1996, this author distinguished between engineering resilience and ecological resilience, where the former refers to the capacity to resist a disturbance and the speed with which the previous equilibrium state is recovered, and the latter indicates the magnitude of the disturbance absorbed before a system changes to a subsequent state [18]. Other authors have defined ecological resilience as the capacity of a system to resist and recover from a disturbance [19]. Despite these potential confusions in terminology, the use of the term resilience has significantly increased in recent decades, with an average rise of 7.46% per year between 1984 and 2014. Contrary to this, the frequency of use of the words resistance and recovery decreased by 1.01% and 0.86% during the same period [19].

Studies on marine species have accumulated evidence that genetic diversity increases resistance, resilience, and productivity. However, studies regarding benthic species are scarce [5, 7, 20, 21]. The objective of this review is to synthetize results from scientific studies related to benthic marine species that have evaluated the existence of a relationship between genetic diversity and resilience capacity.

Method

This review presents results from studies that evaluated the existence of relationships or effects between genetic diversity and resilience capacity in populations of marine benthic species. In this review, the term resilience refers to “the capacity of a system to resist and to recover from a disturbance”, as recommended by Hodgson (2015) [19]. Studies included are only those in which genetic diversity was the variable or independent factor or predictor variable, and resilience was the dependent response variable. Empirical studies included laboratory and field experiments. The analysis excluded theoretical studies and those that did not use molecular analyses of genetic diversity. References from previous reviews were considered, as well as articles complying with the above-mentioned criteria.

Studies were searched using the web sites Science Direct, Web of Knowledge, Scopus and Mendeley. The key words employed were resilience, resistance, recovery, genetic diversity, population, benthic, marine and disturbance. The articles extracted from the search underwent three evaluation stages to be selected or eliminated. Main titles and summaries were assessed in the first stage; methodologies and results from the first stage selection were assessed in second stage; and studies selected in the third stage were subject to complete revision.

From the selected articles, we extracted methodological information on type of research (experiment, field experiment or field study), duration of the study, molecular genetic marker used, species studied, unit of measurement for genetic diversity (variable or predictor factor), type of disturbance (treatment), and unit of measurement for resilience (response variable). The relationships or effects of genetic diversity on resilience capacity after disturbances were classified as positive, negative, or without relation. By aggregating the information from all the studies, we estimated the percentages of results showing positive, negative, or no relation between genetic diversity and resilience, and highlighted the types of measurements used the most. Finally, we described an underlying mechanism that could explain the findings, as commonly outlined by the studies that considered this type of analysis.

Results

The search and selection of studies regarding the existence of a relationship or an effect between genetic diversity and resilience capacity in benthic marine species unearthed twenty-five publications between 2001 and 2018, six of which were published in the last year. The publications included 13 species as follows: Eight sea-grass species (Zostera marina, Z. muelleri and Z. noltii, Posidonia australis, P. oceanica, Vallisneria americana, Phragmites australis and Spartina alterniflora); three sea-weed species (Gracilaria chilensis, G. vermiculophylla and Ecklonia radiata); one oyster (Crassostrea virginica), and one crustacean (Americamysis bahia). 84% of the publications were related to sea-grass species, among which Z. marina was the most studied (32% of publications) (Fig. 1, See also Table 1 Add file). The methodologies included 12 laboratory experiments (48%), 9 field experiments (36%), and 4 field studies (16%) (Fig. 1). The duration of the studies varied between three weeks and three years, and only one lasted more than two years (Fig. 1). The genetic markers used for genetic diversity analyses were microsatellites (SSR) in 88% of the studies; alloenzymes in 4%, Amplified Fragment Length Polymorphism (AFLP) in 4%, and Single Nucleotide Polymorphism (SNP) in 4% (Fig. 1). All studies included 22 measures of genetic diversity that are detailed in Table 1. Resilience was evaluated with nearly 50 different direct and indirect measures for resistance and recovery. The types of disturbances that were studied the most were variations in temperature, light, nutrients, and herbivores, as well as the effects of transplantation and/or relocation. Survival, growth, biomass, density and recruitment were the most frequently resilience measures found (See Table 1, Add file).

Fig. 1
figure 1

Publications Methodology: Percentage of publications according to study type (experiment, field experiment, field study), study duration (in months), genetic marker (SSR, SNP, AFLP, alloenzymes) and species studied

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Table 1 Measures of genetic diversity used to evaluate resilience capacity in the studies included in this review
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The number of tests used to evaluate the relationship or effect between genetic diversity and resilience capacity ranged from 1 to 23. Consequently, many studies presented results with more than one type of relationship between genetic diversity and resilience capacity, depending on how genetic diversity and resilience were measure (Fig. 2). In total, the studies included 150 analyses, using different combinations of measures for genetic diversity (predictor variable) and resilience (response variable). Among the analyses, 44% found positive relationships between genetic diversity and resilience capacity, 6% found negative relationships, and 50% found no relation (Fig. 3). The genetic diversity measure that was used the most to evaluate resilience was multi-locus genotype (MLG), where 60% of studies that used this measure found positive relations, 2% found negative relations, and 38% found no relation. Allele richness (AR) was the second most used measure, resulting in 42% positive relationships, 11% negative, and 47% no relationship with resilience. Genotypic diversity (R) was the third most used measure, yielding 20% positive relationships, 20% negative, and 60% no relationship with resilience (Fig. 4).

Fig. 2
figure 2

Genetic Diversity and Resilience Relationship: Percentages (%) of the type of relationship or effect between genetic diversity and resilience; Positive (blue), Negative (black) and No Relationship (grey) with the number of measurements (red line) for each study

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Fig. 3
figure 3

Total Genetic Diversity and Resilience Relationship: Percentages (%) of the type of relationship or effect between genetic diversity and resilience; Positive (blue), Negative (black) and No Relationship (grey) out of all measures (N = 150)

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Fig. 4
figure 4

Genetic Diversity Measure and Resilience Relationship: Percentage (%) of relationship or effect between genetic diversity and resilience capacity; Positive (blue), Negative (black) and No Relationship (grey). MLG = Multi-locus genotype, R = Genotypic diversity, PLP = Percentage of polymorphic loci, NHL = Number of heterozygous loci, H = Heterozygosity, Ho = Observed heterozygosity, He = Expected heterozygosity, Hj = Heterozygosity, Hnb = Unbiased heterozygosity, Diploid, Heterozygous (MDH y GPI-2), Heterozygous (MDH), Heterozygous (GPI-2), AR = Allele richness, D. Cohort = Cohort diversity, GR = Genetic relatedness, Fis = Inbreeding coefficient, Pareto B, Pareto Max, D = Simpson’s genotype diversity index, CR = Clonal sub range, NHL-MLG, MLG-AR, PLP-Hj and Set = MLG, R, AR, Na, Ho and He. See also Table 1 for definitions

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The measure that was used the most to analyze resilience with respect to genetic diversity was population density, where there were positive relationships 61% of the time, and no relationship 39% of the time. Daily growth rate was the second most used measure for resilience, for which 33% of the results were positive, 7% negative, and 60% found no relation with genetic diversity. Finally, survivability was the third most used measure, which resulted in 62% positive relationships, 23% negative, and 15% no relation with genetic diversity (Fig. 5).

Fig. 5
figure 5

Resilience Measures and Genetic Diversity: Percentages (%) of the types of relationship or effect between genetic diversity and resilience capacity: Positive (blue), Negative (black) and No Relationship (grey) for each measure or resilience. For details of these resilience measures, see also references number [5,6,7, 20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44]

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There were seven studies (39%) that examined the mechanism underlying the relationship between genetic diversity and resilience capacity, all of which used Microsatellites (SSR) to evaluate genetic diversity. Six studies emphasized on a mechanism that combined the effect of natural selection (dominance) and complementarity, and one study only highlighted complementarity.

Discussion and conclusions

Despite evidence suggesting the importance of genetic diversity for individual survival, population persistence and the functioning of communities and ecosystems, few studies were found regarding benthic marine species (N = 25). These studies gradually increased between 2001 and 2018 (nearly two decades), although there were 6 publications in the last year. There were clearly more studies on sea-grass and marine sea-weed species (84%), particularly on the species Zostera marina (32%).

The effects of genetic diversity on resilience were variable dependent. Most of the studies found more than one relationship, depending on the resilience measure and the measure of genetic diversity employed. When analyzing the results by variable, independent of the study, more positive relationships between genetic diversity and resilience were found (44%) compared to negative relationships, which were few (6%). No relationship between genetic diversity and resilience was found in 50% of the analyzed cases.

Positive relationships between genetic diversity and resilience were associated with greater survival, growth and physiological versatility under disturbances such as number of contaminators, salinity, alterations in temperature, and so forth. For instance, genetic diversity was related to increases in resistance to transplantation and herbivores in Z. marina [5], as well as to better recovery rates, densities and biomass after temperature changes [7, 21, 22]. Populations of the alga Ecklonia radiata with greater genetic diversity had more growth and physiological versatility under heat waves [23]. The crustacean Americamys bahia showed higher fitness and adaptation capacities with changes in salinity, presenting higher genetic diversity [24]. One recent experiment on the marine plant Cymodocea nodosa showed that resistance to lack of light increased significantly with genetic diversity, and that recovery was conditioned by this resistance [42].

Negative relationships between diversity and resilience were associated with mortality, net growth, biomass and survivability. Sea-grass beds of Posidonia oceanica with low genetic diversity were more resistant to pisciculture [44]. Although the mechanism was not evaluated, the authors related these results to the existence of large and dominant clones that would have been selected over a long period of time due to phenotypic plasticity, thus causing low genetic diversity and/or exclusion by competition. Any of these processes should provide resistance advantages under short-term environmental disturbances such as fish farming. However, the authors also recognized a potential bias due to the absence of genetic data prior to the disturbance, thus suggesting more laboratory experiments. This study [44] conducted the highest number of evaluations (N = 23) on measures for genetic diversity and resilience. Only four of these evaluations found negative effects or relationships, whereas no relationship or effects were found in the others. Regarding Posidonia australis, a negative relationship was also found between genetic diversity and two of the seven measures for resilience employed (area and leaf growth rate) [25].

One of the studies where no relationship was found between genetic diversity and resilience was conducted by Macreadie et al. (2014) [26] on populations of Z. muelleri. They concluded that population recovery for this species after small-scale disturbances would depend on the growth of the clones, and that sexual reproduction would have little or no relevance. In Z. marina, recovery after an extreme disturbance initially would have been by sexual reproduction via germination of a seed bank. However, later recovery was accompanied by vegetative growth, decreasing genotype diversity. Despite this, genetic diversity among new sea-grass beds remained high. This proves the importance of sexual reproduction in the recovery and persistence of these beds [43].

Sexual reproduction provides genetic variation by segregation and recombination, while asexual reproduction provides genetic variation only by recombination. Consequently, populations with sexual reproduction show more genetic variation than asexual populations. However, there is evidence that sexual reproduction can also cause a decrease in genetic variation [45]. The mixture of reproductive modes can produce flexibility, allowing genotypes locally adapted to favorable environments to multiply rapidly by clonal propagules. Alternatively, the mixture of gametes may provide the genetic novelties necessary for the colonization of new habitats [46, 47]. The maintenance of alternative reproductive methods allows for the persistence of populations in unpredictable environments or highly fluctuating conditions [48]. The classic model of clonal propagation dynamics suggests a relationship between genetic diversity and physical disturbances, where genotype richness is low (high clonality) in stable environments and high (low clonality) in disturbed environments [43, 46, 49].

No effects of heterozygosity were found on growth or physiological responses in populations of Gracilaria chilensis. These results are likely to be connected to historical domestication, which would have limited genetic diversity in these cultivated populations. However, no evaluations of these proposed mechanisms were found [27]. The relationship between genetic diversity and resilience depends on the environmental conditions. The magnitude and direction of these effects vary depending on the measure of genetic diversity used [28] and on the biological characteristics of the species, as well as the methodology used. The absence of a relationship in some studies may be due to methodological design, the selection of measures for genetic diversity and resilience, the type and number of genetic markers, the duration of the study or other reasons. For example, the observed heterozygosity, the Simpson index of genotypic diversity, and the fixation indices found no relationship with any of the measures for resilience. Chlorophyll and phenol concentration and structures, like the turion, reflected no relations with any of the measures of genetic diversity. Capdevilla et al. (2021) recommended using common and comparable resilience measures [50]. This recommendation has not yet been accepted, since there is currently a dispute about which definition is to be used, and new definitions continue to appear [51].

Only 39% of the reviewed studies evaluated the underlying mechanisms of the relationship between genetic diversity and resilience capacity. These results mainly highlighted a combined effect of natural selection and complementarity. Microsatellites were used in all studies that analyzed genetic diversity. The use of neutral molecular markers has been a constant topic of discussion in evaluating the effect of genetic diversity on resilience, given that neutral variation by definition does not have ecological consequences, which is why this type of marker has no adaptive potential [22, 26, 29, 52, 53]. Nevertheless, the theory of biological heterozygosity-fitness, inferred from neutral markers, can be interpreted as a result of a general effect on the genome (“the general effect hypothesis”) or as a local effect in a unique locus (“the local effect hypothesis”) [54]. New tools, such as Next-Generation Sequencing (NGS), are more appropriate for the study of gene expression with adaptive importance [52]. Differentiating between the underlying mechanisms related to diversity effects, such as complementarity and selection, is fundamental, given that these effects help identify the processes that connect genetic diversity and demographic traits [28, 55].

The results of this review demonstrate that the relationship between genetic diversity and resilience is mainly positive. Genetic diversity tended to increase the resistance and recovery capacity of benthic marine populations after natural perturbations such as heat waves and algal blooms, as well as after anthropic disturbances such as marine eutrophication. This reinforces the importance of acknowledging and maintaining genetic diversity for the conservation of populations in marine ecosystems. Its loss might lead to decreases in physiological versatility and in resilience capacity, while also causing a cascading effect towards lower biodiversity levels, which could become critical and cause potentially irreversible changes in the structure and functioning of ecosystems [23]. Maintaining resilience and the adaptive capacity of marine ecosystems by conserving genetic diversity must be a central component of efforts in the current decade, which the United Nations has declared the Decade of the Oceanographic Sciences for Sustainable Development [56].

Availability of data and materials

The datasets used in the current study are available from the corresponding author on reasonable request.

Abbreviations

DIN:

Dissolved Inorganic Nitrogen

References

  1. O’Leary JK, Micheli F, Airoldi L, Boch C, De Leo G, Elahi R, et al. The resilience of marine ecosystems to climatic disturbances. Bioscience. 2017;67(3):208–20. https://doi.org/10.1093/biosci/biw161.

  2. Jump AS, Marchant R, Peñuelas J. Environmental change and the option value of genetic diversity. Trends Plant Sci. 2009;14(1):51–8. https://doi.org/10.1016/j.tplants.2008.10.002.

  3. Tepolt CK, Grosholz ED, de Rivera CE, Ruiz GM. Balanced polymorphism fuels rapid selection in an invasive crab despite high gene flow and low genetic diversity. Mol Ecol. 2022;31(1):55–69. https://doi.org/10.1111/mec.16143.

  4. Teixeira JC, Huber CD. The inflated significance of neutral genetic diversity in conservation genetics. Proc Natl Acad Sci U S A. 2021;118(10):1–10.

    Article  Google Scholar 

  5. Hughes AR, Stachowicz JJ. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci. 2004;101(24):8998–9002. https://doi.org/10.1073/pnas.0402642101.

  6. Salo T, Gustafsson C. The Effect of Genetic Diversity on Ecosystem Functioning in Vegetated Coastal Ecosystems. Ecosystems. 2016;19(8):1429–44. https://doi.org/10.1007/s10021-016-0014-y.

  7. Reusch T, Ehlers A, Hammerli A, Worm B. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. PNAS. 2005;102(8):2826–31. https://doi.org/10.1073/pnas.0500008102.

  8. Shull GH. What Is “Heterosis”? Genetics. 1948;33(5):439–46. https://doi.org/10.1093/genetics/33.5.439.

  9. East EM. Heterosis. Genetics. 1936;21(July):375.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Milton J., Grant M. Associations Among Protein Heterozygosity, Growth Rate, And Developmental Homeostasis. Annu Rev Ecol Syst. 1984;15:479–99. https://doi.org/10.1146/annurev.es.15.110184.002403.

  11. Chen ZJ. Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet. 2013;14(7):471–82. https://doi.org/10.1038/nrg3503.

  12. Liu N, Du Y, Warburton ML, Xiao Y, Yan J. Phenotypic plasticity contributes to maize adaptation and heterosis. Mol Biol Evol. 2020;38(4):1262–1275. https://doi.org/10.1093/molbev/msaa283.

  13. Templeton AR, Hemmer H, Mace G, Seal US, Shields WM, Woodruff DS. Local adaptation, coadaptation, and population boundaries. Zoo Biol. 1986;5(2):115–25. https://doi.org/10.1002/zoo.1430050206.

  14. Hairston NG, Ellner SP, Geber MA, Yoshida T, Fox JA. Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett. 2005;8(10):1114–27. https://doi.org/10.1111/j.1461-0248.2005.00812.x.

  15. Kokko H, López-Sepulcre A. The ecogenetic link between demography and evolution: Can we bridge the gap between theory and data? Ecol Lett. 2007;10(9):773–82. https://doi.org/10.1111/j.1461-0248.2007.01086.x.

  16. Richardson DM, Pyšek P. Elton, C.S. 1958: The ecology of invasions by animals and plants. London: Methuen. Prog Phys Geogr. 2007;31(6):659–66. https://doi.org/10.1177/0309133307087089.

  17. Holling CS. Resilience And Stability of Ecological Systems. Annu Rev Ecol Syst. 1973;4:1–23. https://doi.org/10.1146/annurev.es.04.110173.000245.

  18. Holling CS. Engineering resilience versus ecological resilience. Eng Within Ecol Constraints. 1996;1996:31–43.

    Google Scholar 

  19. Hodgson D, McDonald JL, Hosken DJ. What do you mean, “resilient”? Trends Ecol Evol. 2015;30(9):503–6. https://doi.org/10.1016/j.tree.2015.06.010.

  20. Massa SI, Paulino CM, Serrão EA, Duarte CM, Arnaud-Haond S. Entangled effects of allelic and clonal (genotypic) richness in the resistance and resilience of experimental populations of the seagrass Zostera noltii to diatom invasion. BMC Ecol. 2013;13:39. https://doi.org/10.1186/1472-6785-13-39.

  21. Ehlers A, Worm B, Reusch TBH. Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Mar Ecol Prog Ser. 2008;355:1–7. https://doi.org/10.3354/meps07369.

  22. Hughes AR, Brian D, Johnson MTJ, Underwood N. Ecological consequences of genetic diversity. Ecol Lett. 2008;11:609–23. https://doi.org/10.1111/j.1461-0248.2008.01179.x.

  23. Wernberg T, Coleman MA, Bennett S, Thomsen MS, Tuya F, Kelaher BP. Genetic diversity and kelp forest vulnerability to climatic stress. Sci Rep. 2018;8:1851. https://doi.org/10.1038/s41598-018-20009-9.

  24. Markert JA, Champlin DM, Gutjahr-Gobell R, Grear JS, Kuhn A, McGreevy TJ, et al. Population genetic diversity and fitness in multiple environments. BMC Evol Biol. 2010;10(1):5–9. https://doi.org/10.1186/1471-2148-10-205.

  25. Evans SM, Sinclair EA, Poore AGB, Bain KF, Vergés A. Assessing the effect of genetic diversity on the early establishment of the threatened seagrass Posidonia australis using a reciprocal-transplant experiment. Restor Ecol. 2018;26(3):570–80. https://doi.org/10.1111/rec.12595.

  26. Macreadie PI, York PH, Sherman CDH. Resilience of Zostera muelleri seagrass to small-scale disturbances: The relative importance of asexual versus sexual recovery. Ecol Evol. 2014;4(4):450–61. https://doi.org/10.1002/ece3.933.

  27. Usandizaga S, Camus C, Kappes JL, Guillemin ML, Buschmann AH. Nutrients, but not genetic diversity, affect Gracilaria chilensis (Rhodophyta) farming productivity and physiological responses. J Phycol. 2018;54:860–869. https://doi.org/10.1111/jpy.12785.

  28. Hanley TC, Hughes AR, Williams B, Garland H, Kimbro DL. Effects of intraspecific diversity on survivorship, growth, and recruitment of the eastern oyster across sites. Ecology. 2016;97(6):1518–29. https://doi.org/10.1890/15-1710.1.

  29. Hughes RA, Stachowicz JJ. Seagrass genotypic diversity increases disturbance response via complementarity and dominance. J Ecol. 2011;99(2):445–53. https://doi.org/10.1111/j.1365-2745.2010.01767.x.

  30. Schrandt M, Powers S, Scott Rikard F, Thongda W, Peatman E. Short-term low salinity mitigates effects of oil and dispersant on juvenile eastern oysters: A laboratory experiment with implications for oil spill response activities. PLoS ONE. 2018;13:1–16. https://doi.org/10.1371/journal.pone.0203485.

    Article  CAS  Google Scholar 

  31. Gallegos Sánchez CF, Beltrán J, Flores V, González AV, Santelices B. Testing the effects of heterozygosity on growth rate plasticity in the seaweed Gracilaria chilensis (Rhodophyta). Ecol Evol. 2018;8:5741–51. https://doi.org/10.1002/ece3.4113.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Connolly RM, et al. Highly disturbed populations of seagrass show increased resilience but lower genotypic diversity. Front Plant Sci. 2018;9:1–9. https://doi.org/10.3389/fpls.2018.00894.

    Article  Google Scholar 

  33. Evans SM, Vergés A, Poore AGB. Genotypic diversity and short-term response to shading stress in a threatened seagrass: Does low diversity mean low resilience? Front Plant Sci. 2017;8:1–11. https://doi.org/10.3389/fpls.2017.01417.

    Article  Google Scholar 

  34. Gerstenmaier CE, Krueger-Hadfield SA, Sotka EE. Genotypic diversity in a non-native ecosystem engineer has variable impacts on productivity. Mar Ecol Prog Ser. 2016;556:79–89. https://doi.org/10.3354/meps11809.

    Article  Google Scholar 

  35. Tomimatsu H, Nakano K, Yamamoto N, Suyama Y. Effects of genotypic diversity of Phragmites australis on primary productivity and water quality in an experimental wetland. Oecologia. 2014;175:163–72. https://doi.org/10.1007/s00442-014-2896-8.

    Article  PubMed  Google Scholar 

  36. Wang XY, et al. Genotypic diversity enhances invasive ability of Spartina alterniflora. Mol Ecol. 2012;21:2542–51. https://doi.org/10.1111/j.1365-294X.2012.05531.x.

    Article  CAS  PubMed  Google Scholar 

  37. Reynolds LK, McGlathery KJ, Waycott M. Genetic diversity enhances restoration success by augmenting ecosystem services. PLoS ONE. 2012;7:1–7. https://doi.org/10.1371/journal.pone.0038397.

    Article  CAS  Google Scholar 

  38. Hughes AR, Stachowicz JJ. Ecological impacts of genotypic diversity in the clonal seagrass Zostera marina. Ecology. 2009;90:1412–9. https://doi.org/10.1890/07-2030.1.

    Article  PubMed  Google Scholar 

  39. Diaz-Almela E, et al. Feed-backs between genetic structure and perturbation-driven decline in seagrass (Posidonia oceanica) meadows. Conserv Genet. 2007;8:1377–91. https://doi.org/10.1007/s10592-007-9288-0.

    Article  Google Scholar 

  40. Williams SL. Reduced Genetic Diversity in Eelgrass Transplantations Affects both Population Growth and Individual Fitness. Ecol Appl. 2001;11:1472–88. https://doi.org/10.2307/3060933.

    Article  Google Scholar 

  41. Engelhardt KAM, Lloyd MW, Neel MC. Effects of genetic diversity on conservation and restoration potential at individual, population, and regional scales. Biol Conserv. 2014;179:6–16. https://doi.org/10.1016/j.biocon.2014.08.011.

    Article  Google Scholar 

  42. Tuya F, Fernández-Torquemada Y, del Pilar-Ruso Y, Espino F, Manent P, Curbelo L, et al. Partitioning resilience of a marine foundation species into resistance and recovery trajectories. Oecologia. 2021;196(2):515–27. https://doi.org/10.1007/s00442-021-04945-4.

  43. Paulo D, Diekmann O, Ramos AA, Alberto F, Serrão EA. Sexual reproduction vs. Clonal propagation in the recovery of a seagrass meadow after an extreme weather event. Sci Mar. 2019;83(4):357–63. https://doi.org/10.3989/scimar.04843.06A.

  44. Arnaud-Haond S, Marbà N, Diaz-Almela E, Serrão EA, Duarte CM. Comparative analysis of stability-genetic diversity in seagrass (Posidonia oceanica) meadows yields unexpected results. Estuaries and Coasts. 2010;33(4):878–89. https://doi.org/10.1007/s12237-009-9238.

  45. Gorelick R, Heng HHQ. Sex reduces genetic variation: A multidisciplinary review. Evolution (N Y). 2011;65(4):1088–98. https://doi.org/10.1111/j.1558-5646.2010.01173.x.

  46. Williams G. Sex and Evolution. Princeton, New Jersey: Princeton University Press; 1975.

    Google Scholar 

  47. Jackson JBC. Modes of dispersal of clonal benthic invertebrates: consequences for species’ distributions and genetic structure of local populations. Bull Mar Sci. 1986;39(2):588–606.

    Google Scholar 

  48. Torres AF, Forsman ZH, Ravago-Gotanco R. Shifts in coral clonality along a gradient of disturbance: insights on reproduction and dispersal of Pocillopora acuta. Mar Biol. 2020;167(161):1–18. https://doi.org/10.1007/s00227-020-03777-9.

  49. Connell JH. Diversity in Tropical Rain Forests and Coral Reefs High diversity of trees and corals is maintained. Science. 1978;199(4335):1302–10. https://doi.org/10.1126/science.199.4335.1302.

  50. Capdevila P, Stott I, Oliveras Menor I, Stouffer DB, Raimundo RLG, White H, et al. Reconciling resilience across ecological systems, species and subdisciplines. J Ecol. 2021;109(9):3102–13. https://doi.org/10.1111/1365-2745.13775.

  51. Oliver D. Idenity of ecological systems and the meaning of resilience.pdf. J Ecol. 2021;109:3147–56. https://doi.org/10.1111/1365-2745.13655.

  52. Kirk H, Freeland JR. Applications and implications of neutral versus non-neutral markers in molecular ecology. Int J Mol Sci. 2011;12(6):3966–88. https://doi.org/10.3390/ijms12063966.

  53. Whitlock R. Relationships between adaptive and neutral genetic diversity and ecological structure and functioning: A meta-analysis. J Ecol. 2014;102(4):857–72. https://doi.org/10.1111/1365-2745.12240.

  54. Kempenaers B. Mate Choice and Genetic Quality: A Review of the Heterozygosity Theory. Adv Study Behav. 2007;37(07):189–278. https://doi.org/10.1016/S0065-3454(07)37005-8.

  55. Loreau M, Hector A. Partitioning selection and complementarity in biodiversity experiments. Nature. 2001;412(6842):72–6.

    Article  CAS  PubMed  Google Scholar 

  56. Thomson AI, Archer FI, Coleman MA, Gajardo G, Goodall-Copestake WP, Hoban S, et al. Charting a course for genetic diversity in the UN Decade of Ocean Science. Evol Appl. 2021;14(6):1497–518. https://doi.org/10.1111/eva.13224.

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Acknowledgements

Cynthia Vásquez thanks to PhD Program in Systematics and Biodiversity of University of Concepción, for the support provided while developing this study. The authors would like to thank two anonymous reviewers whose comments and suggestions greatly improved the manuscript.

Funding

This study was funded by the Interdisciplinary Center for Aquaculture Research (INCAR, FONDAP-ANID, Grants Nº15110027 and 1522A0004). The funders had no role in the study design, data collection, analysis, decision to publish or preparation of the manuscript.

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Authors and Affiliations

  1. Interdisciplinary Center for Aquaculture Research (INCAR), Universidad de Concepción, Concepción, Chile

    Cynthia Vásquez, Renato A. Quiñones & Eduardo Hernández-Miranda

  2. Programa de Doctorado en Sistemática y Biodiversidad, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

    Cynthia Vásquez

  3. Departamento de Oceanografía, Universidad de Concepción, Casilla 160-C, Concepción, Chile

    Renato A. Quiñones

  4. Departamento de Ecología, Facultad de Ciencias, Universidad Católica de La Santísima Concepción, Concepción, Chile

    Antonio Brante & Eduardo Hernández-Miranda

  5. Laboratorio de Investigación en Ecosistemas Acuáticos (LInEA), Concepción, Chile

    Eduardo Hernández-Miranda

Authors
  1. Cynthia Vásquez
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  2. Renato A. Quiñones
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  3. Antonio Brante
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  4. Eduardo Hernández-Miranda
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Contributions

CV: Conceptualization, Methodology, Formal analysis, Investigation, Writing Original Draft. RQ: Writing—Review & Editing. AB: Writing—Review & Editing. EHM: Conceptualization, Methodology, Writing—Review & Editing. All authors read and approved the final manuscript.

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Correspondence to Eduardo Hernández-Miranda.

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Supplementary Information

Additional file 1:

Table 1. Comparative synthesis of scientific studies included in this review.

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Vásquez, C., Quiñones, R.A., Brante, A. et al. Genetic diversity and resilience in benthic marine populations. Rev. Chil. de Hist. Nat. 96, 4 (2023). https://doi.org/10.1186/s40693-023-00117-1

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Revista Chilena de Historia Natural

ISSN: 0717-6317

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