Vol.:(0123456789)1 3 Conservation Genetics (2021) 22:533–536 https://doi.org/10.1007/s10592-021-01359-w LETTER TO THE EDITOR Authors’ Reply to Letter to the Editor: Continued improvement to genetic diversity indicator for CBD Linda Laikre1 · Paul A. Hohenlohe2 · Fred W. Allendorf3 · Laura D. Bertola4 · Martin F. Breed5 · Michael W. Bruford6 · W. Chris Funk7 · Gonzalo Gajardo8 · Antonio González‑Rodríguez9 · Catherine E. Grueber10 · Philip W. Hedrick11 · Myriam Heuertz12 · Margaret E. Hunter13 · Kerstin Johannesson14 · Libby Liggins15 · Anna J. MacDonald16 · Joachim Mergeay17,18 · Farideh Moharrek19,20 · David O’Brien21 · Rob Ogden22 · Pablo Orozco‑terWengel6 · Clarisse Palma‑Silva23 · Jennifer Pierson24 · Ivan Paz‑Vinas25 · Isa‑Rita M. Russo6 · Nils Ryman1 · Gernot Segelbacher26 · Per Sjögren‑Gulve27 · Lisette P. Waits28 · Cristiano Vernesi29 · Sean Hoban30 Accepted: 24 March 2021 / Published online: 22 April 2021 © The Author(s) 2021 We appreciate the encouraging response to our call for indicators for genetic diversity within the post-2020 Global Biodiversity Framework of the Convention on Biological Diversity, CBD (Laikre et al. 2020; Hoban et al. 2020). In agreement with us, Frankham (2021) highlights the urgent necessity for the CBD to include an indicator that tracks the maintenance of genetic diversity within populations of all species—wild and domestic. Draft CBD Headline indicators (which all CBD Parties will need to report) do not include genetic diversity within populations of wild species (CBD/ SBSTTA/24/3Add.1). The genetically effective population size (Ne) is a metric that quantifies the rate of genetic change within a population. We welcome Frankham’s (2021) comments on the relevance of this important parameter, and the appropriate indicator threshold (Ne > 500 or Nc > 5000; Nc = adult census size, the This reply refers to the comment available online at https:// doi. org/ 10. 1007/ s10592- 021- 01357-y. * Linda Laikre linda.laikre@popgen.su.se * Sean Hoban shoban@mortonarb.org Paul A. Hohenlohe hohenlohe@uidaho.edu Fred W. Allendorf fred.allendorf@gmail.com Laura D. Bertola laura.bertola@gmail.com Martin F. Breed martin.breed@flinders.edu.au Michael W. Bruford BrufordMW@Cardiff.ac.uk W. Chris Funk Chris.Funk@colostate.edu Gonzalo Gajardo ggajardo@ulagos.cl Antonio González-Rodríguez agrodrig@iies.unam.mx Catherine E. Grueber catherine.grueber@sydney.edu.au Philip W. Hedrick PHILIP.HEDRICK@asu.edu Myriam Heuertz myriam.heuertz@inrae.fr Margaret E. Hunter mhunter@usgs.gov Kerstin Johannesson Kerstin.Johannesson@gu.se Libby Liggins L.Liggins@massey.ac.nz Anna J. MacDonald anna.macdonald@anu.edu.au Joachim Mergeay joachim.mergeay@inbo.be Farideh Moharrek farideh.moharrek@sund.ku.dk David O’Brien David.OBrien@nature.scot Rob Ogden Rob.Ogden@ed.ac.uk http://crossmark.crossref.org/dialog/?doi=10.1007/s10592-021-01359-w&domain=pdf https://doi.org/10.1007/s10592-021-01357-y https://doi.org/10.1007/s10592-021-01357-y 534 Conservation Genetics (2021) 22:533–536 1 3 Pablo Orozco-terWengel orozco-terwengelpa@cardiff.ac.uk Clarisse Palma-Silva clarissepalma@gmail.com Jennifer Pierson Jennifer.Pierson@australianwildlife.org Ivan Paz-Vinas ivanpaz23@gmail.com Isa-Rita M. Russo russoim@cardiff.ac.uk Nils Ryman nils.ryman@popgen.su.se Gernot Segelbacher gernot.segelbacher@wildlife.uni-freiburg.de Per Sjögren-Gulve Per.Sjogren-Gulve@naturvardsverket.se Lisette P. Waits lwaits@uidaho.edu Cristiano Vernesi cristiano.vernesi@fmach.it 1 Division of Population Genetics, Department of Zoology, Stockholm University, SE 10691 Stockholm, Sweden 2 Institute for Bioinformatics and Evolutionary Studies, Department of Biological Sciences, University of Idaho, 875 Perimeter Drive MS 3051, Moscow, ID 83844-3051, USA 3 Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA 4 City College of New York, 160 Convent Ave., New York, NY 10031, USA 5 College of Science and Engineering, Flinders University, Bedford Park, SA 5042, Australia 6 School of Biosciences, Cardiff University, Cardiff CF10 3AX, Wales, UK 7 Graduate Degree Program in Ecology, Department of Biology, Colorado State University, Fort Collins, CO, USA 8 Universidad de Los Lagos, Lab Genetics, Aquaculture & Biodiversity, Osorno, Chile 9 Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia, Michoacán, Mexico 10 School of Life and Environmental Sciences, Faculty of Science, The University of Sydney, Sydney, NSW 2006, Australia 11 School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA 12 INRAE, Univ. Bordeaux, Biogeco, 69 route d’Arcachon, 33610 Cestas, France 13 U.S. Geological Survey, Wetland and Aquatic Research Center, 7920 NW 71st St, Gainesville, FL 32653, USA 14 Department of Marine Sciences, University of Gothenburg, Tjärnö, Strömstad, Sweden 15 School of Natural and Computational Sciences, Massey University, Auckland, New Zealand 16 The John Curtin School of Medical Research/Research School of Biology, The Australian National University, Acton, ACT  2601, Australia 17 Research Institute for Nature and Forest, Gaverstraat 4, 9500 Geraardsbergen, Belgium 18 Aquatic Ecology, Evolution and Conservation, KULeuven, Charles Deberiotstraat 32, box 2439, 3000 Leuven, Belgium 19 Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Blegdamsvej 3B, 2200 Copenhagen, Denmark 20 Faculty of Biological Sciences, Tarbiat Modares University, Tehran 14115-154, Iran 21 Scottish Natural Heritage, Leachkin Road, Inverness IV3 8NW, UK 22 Royal (Dick) School of Veterinary Studies and the Roslin Institute, University of Edinburgh, Easter Bush Campus, EH25 9RG Midlothian, UK 23 Department of Plant Science, Institute of Biology, University of Campinas, Campinas, SP 13083-862, Brazil 24 Australian Wildlife Conservancy, PO Box 8070, Subiaco East WA 6008, Australia 25 Laboratoire Evolution & Diversité Biologique, Centre National pour la Recherche Scientifique, Institut de Recherche pour le Développement, Université Toulouse III Paul Sabatier, UMR-5174 EDB, Toulouse, 118 route de Narbonne, 31062 Toulouse, France 26 Wildlife Ecology and Management, University Freiburg, Tennenbacher Str. 4, 79106 Freiburg, Germany 27 The Wildlife Analysis Unit, The Swedish Environmental Protection Agency, 10648 Stockholm, Sweden 28 Department of Fish and Wildlife Sciences, University of Idaho, Moscow, ID 83844, USA 29 Department of Sustainable Agroecosystems and Bioresources, Research and Innovation Centre - Fondazione Edmund Mach, via E. Mach 1, 38010 S. Michele All’Adige, TN, Italy 30 Center for Tree Science, The Morton Arboretum, 4100 Illinois Rt 53, Lisle 60532, USA 535Conservation Genetics (2021) 22:533–536 1 3 number of sexually mature individuals). Frankham (2021) suggests rewording our proposed indicator 1, “The number of populations [or breeds] within species with an effective population size > 500 compared to the number < 500”, to “The number of populations (or breeds) with > 5000 mature individuals compared to the number < 5000.” The proposed rephrasing coincides with our suggestion that in the absence of empirical knowledge on Ne, the relationship Ne/Nc ≈ 0.1 can be assumed, substituting Nc ≈ 5000 for Ne ≈ 500 (Fig. 1). We included published estimates of Ne from many popula- tions (Hoban et al. 2020, 2021), recognizing they were not always directly comparable depending on methods used; we appreciate Frankham’s examination of subsets of estimates, which also supports a ratio of approximately 0.1 for many species. Frankham (2021) proposes that his wording is simpler and more suitable for a policy audience. We agree that Ne may be conceptually challenging, but we remain convinced that, even if Nc > 5000 will often be used as a proxy, the term “genetically effective population size” has important meaning in policy (including the CBD, the EU Biodiversity Strategy, and others) for several reasons: (1) Ne stresses that within-population genetic diversity is the indicator’s focus. We consider it critical to signal to policy makers that census size Nc is not a sufficient met- ric to track how fast a population loses genetic diversity. The recent CBD document CBD/SBSTTA/24/3Add.2 acknowledges this: “While population abundance is a key factor in the maintenance of genetic diversity, it is not a sufficient indicator since it does not account for within-population genetic diversity”. (2) Including Ne could spur CBD Parties to initiate more genetic monitoring efforts that will increase availabil- ity of robust estimates of Ne or taxon-specific Ne/Nc ratios. Also, Ne estimates should rapidly increase with the broadening availability of genomic and bioinfor- matics resources and large-scale databases (Santiago et al. 2020; Lawrence et al. 2019). (3) The CBD has used Ne concepts since it first included threatened animal breeds as an indicator. Livestock breeds have been considered as threatened or endan- gered based on Ne thresholds since at least 1992, when Ne < 200 was used to signal genetic erosion (Maijala 1992). Ne features prominently and is explained in detail in numerous Food and Agriculture Organization manuals, and the US endangered species recovery plan- ning, the zoo community, and others are also already utilizing Ne for monitoring genetic diversity. (4) Although Ne/Nc≈0.1 is an appropriate general esti- mate, Frankham and we ourselves are mindful that there is substantial variation; Frankham et al. (2019) provide a thorough analysis in this context. The indi- cator Ne > 500 represents a reminder that maintaining genetic diversity within populations can sometimes require smaller or larger census sizes than Nc = 5000, and allows the use of adequate Ne/Nc estimates when available. (5) Nc can be even more difficult to estimate than Ne, e.g. in many mobile, nocturnal, subterranean, or otherwise hard to count organisms. Frankham (2021) rightly states that Ne can be complex, but theoretical developments and simulated and empirical data are consistently improving our knowledge and tools (Hössjer et al. 2016; Wang 2016; Ryman et al. 2019; San- tiago et al. 2020). Our approach allows new information to be used to adjust Ne/Nc. In addition, the relationship between ploidy level and loss of diversity is likely not as straightforward as suggested by Frankham. For example, Fig. 1 Conceptual diagram for applying the Ne indicator (Hoban et al. 2020). If direct and robust estimates of Ne are available, they should be used. If only general information is available about factors affecting the ratio of Ne to census popula- tion size (Nc), then this informa- tion should be used to calibrate estimates of Nc from the specific population against the Ne > 500 threshold. If no information is available, the indicator is applied using estimates of Nc with the threshold Nc > 5000, implicitly assuming Ne/Nc = 0.1 What informa�on is available on effec�ve popula�on size (Ne)? Gene�c or demographic es�mates of Ne for this species/popula�on No informa�on Use Ne > 500 Use Nc > 5000 General informa�on on Ne/Nc ra�o in this taxonomic group Apply a taxon- specific Ne/Nc Assume Ne/Nc = 0.01 536 Conservation Genetics (2021) 22:533–536 1 3 approximately 50% of all plant species are polyploids, and most, but not all, polyploids lose diversity at the same rate (1/2Ne) as diploids (Soltis and Soltis 2000). Conservation geneticists worldwide are working together to rapidly provide science-based guidelines for Goals, Tar- gets, and Indicators for the post-2020 CBD framework. The Species Information Centre at the Swedish University of Agricultural Sciences has agreed to test indicators 1 and 2 (Hoban et al. 2020) on taxa from the Swedish Red List, and a G-BiKE (https:// sites. google. com/ fmach. it/g- bike- genet ics- eu/ home) working group is compiling data on indicator 3. We look forward to collaborating with Frankham and others to achieve improved CBD indicators for genetic diversity. Genetic diversity must be conserved as a foundation for all biodiversity, adaptive potential, resilience and nature’s con- tributions to society. Acknowledgments We acknowledge ongoing collaboration with the GEO BON Genetic Composition Working Group, the IUCN Conser- vation Genetics Specialist Group, the Society for Conservation Biol- ogy Conservation Genetics Working Group, and the EU Cost Action Genomic Biodiversity Knowledge for Resilient Ecosystems (G-BiKE). This publication is based upon work from COST Action G-BiKE, sup- ported by COST (European Cooperation in Science and Technology). VR and Formas supported L.L. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the United States Government. Open Access This article is licensed under a Creative Commons Attri- bution 4.0 International License, which permits use, sharing, adapta- tion, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. References Frankham R (2021) Suggested improvements to proposed genetic indicator for CBD. Conserv Genet. https:// doi. org/ 10. 1007/ s10592- 021- 01357-y Frankham R, Ballou JD, Ralls K et al (2019) A practical guide for genetic management of fragmented animal and plant populations. Oxford University Press, Oxford (online Appendix 2). http:// www. oup. co. uk/ compa nion/ Frank hamPG Hoban S, Bruford M, D’Urban Jackson J et al (2020) Genetic diversity targets and indicators in the CBD post-2020 Global Biodiversity Framework must be improved. 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Mol Ecol 25:4692–4711 Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. https://sites.google.com/fmach.it/g-bike-genetics-eu/home https://sites.google.com/fmach.it/g-bike-genetics-eu/home http://creativecommons.org/licenses/by/4.0/ https://doi.org/10.1007/s10592-021-01357-y https://doi.org/10.1007/s10592-021-01357-y http://www.oup.co.uk/companion/FrankhamPG http://www.oup.co.uk/companion/FrankhamPG https://doi.org/10.1038/s41597-019-0024-7 https://doi.org/10.1038/s41597-019-0024-7 Authors’ Reply to Letter to the Editor: Continued improvement to genetic diversity indicator for CBD Acknowledgments References