# Authors' Reply to Letter to the Editor: Continued improvement to genetic diversity indicator for CBD

Linda Laikre, Paul A Hohenlohe, Fred W Allendorf, Laura D Bertola, Martin F Breed, Michael W Bruford, W. Chris Chris Funk, Gonzalo Gajardo, Antonio González-Rodríguez, Catherine E Grueber, et al.

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Linda Laikre, Paul A Hohenlohe, Fred W Allendorf, Laura D Bertola, Martin F Breed, et al. Authors' Reply to Letter to the Editor: Continued improvement to genetic diversity indicator for CBD. Conservation Genetics, 2021, pp.1-4. 10.1007/s10592-021-01359-w. hal-03230524

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# 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

© 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 ($N_e$) 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 ($N_e > 500$ or $N_c > 5000$; $N_c$ = adult census size, the

This reply refers to the comment available online at https://doi.org/10.1007/s10592-021-01357-y.

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Linda Laikre
linda.laikre@popgen.su.se

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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
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.Sjögren-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
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 N_e, the relationship N_e/N_c ≈ 0.1 can be assumed, substituting N_c ≈ 5000 for N_e ≈ 500 (Fig. 1). We included published estimates of N_e from many populations (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 N_e may be conceptually challenging, but we remain convinced that, even if N_c > 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) N_e stresses that within-population genetic diversity is the indicator's focus. We consider it critical to signal to policy makers that census size N_c is not a sufficient metric 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 N_c could spur CBD Parties to initiate more genetic monitoring efforts that will increase availability of robust estimates of N_c or taxon-specific N_c/N_c

ratios. Also, N_e estimates should rapidly increase with the broadening availability of genomic and bioinformatics resources and large-scale databases (Santiago et al. 2020; Lawrence et al. 2019).

(3) The CBD has used N_e concepts since it first included threatened animal breeds as an indicator. Livestock breeds have been considered as threatened or endangered based on N_e thresholds since at least 1992, when N_e < 200 was used to signal genetic erosion (Maijala 1992). N_e features prominently and is explained in detail in numerous Food and Agriculture Organization manuals, and the US endangered species recovery planning, the zoo community, and others are also already utilizing N_e for monitoring genetic diversity.

(4) Although N_c/N_e ≈ 0.1 is an appropriate general estimate, Frankham and we ourselves are mindful that there is substantial variation; Frankham et al. (2019) provide a thorough analysis in this context. The indicator N_c > 500 represents a reminder that maintaining genetic diversity within populations can sometimes require smaller or larger census sizes than N_c = 5000, and allows the use of adequate N_c/N_c estimates when available.

(5) N_c can be even more difficult to estimate than N_e, e.g. in many mobile, nocturnal, subterranean, or otherwise hard to count organisms.

Frankham (2021) rightly states that N_c 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; Santiago et al. 2020). Our approach allows new information to be used to adjust N_c/N_c. In addition, the relationship between ploidy level and loss of diversity is likely not as straightforward as suggested by Frankham. For example,

<figure><img src="image_5.png" /><figcaption>**Fig. 1** Conceptual diagram for applying the N_c indicator (Hoban et al. 2020). If direct and robust estimates of N_c are available, they should be used. If only general information is available about factors affecting the ratio of N_c to census population size (N_c), then this information should be used to calibrate estimates of N_c from the specific population against the N_c > 500 threshold. If no information is available, the indicator is applied using estimates of N_c with the threshold N_c > 5000, implicitly assuming N_c/N_c = 0.1</figcaption></figure>
approximately 50% of all plant species are polyploids, and most, but not all, polyploids lose diversity at the same rate (1/2N<sub>e</sub>) as diploids (Soltis and Soltis 2000).

Conservation geneticists worldwide are working together to rapidly provide science-based guidelines for Goals, Targets, 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-genetics-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 contributions to society.

**Acknowledgments** We acknowledge ongoing collaboration with the GEO BON Genetic Composition Working Group, the IUCN Conservation Genetics Specialist Group, the Society for Conservation Biology 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, supported 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.

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