Conservation Genetics (2020) 21:795–801 https://doi.org/10.1007/s10592-020-01301-6 PERSPECTIVE IUCN Red List and the value of integrating genetics Brittany A. Garner1 · Sean Hoban2 · Gordon Luikart3 Received: 2 January 2020 / Accepted: 4 August 2020 / Published online: 18 September 2020 © The Author(s) 2020 Abstract Many species on endangered species lists such as the IUCN Red List (RL) are categorized using demographic factors such as numbers of mature individuals. Genetic factors are not currently used in the RL even though their explicit consideration, including efective population size (Ne) and expected heterozygosity-loss (H-loss), could improve the assessment of extinc- tion risk. Here, we consider the estimation of Ne and H-loss in the context of RL species. First, we investigate the reporting of number of mature individuals for RL Endangered species, which is needed to estimate Ne and H-loss. We found 77% of species assessments studied here did not report methods used to estimate the number of mature adults, and that these assessments rarely report other important determinants of Ne (e.g., sex ratio, variance in family size). We therefore applied common rules of thumb to estimate Ne, and found that Ne was likely < 50 for at least 25% of the 170 RL Endangered species studied here. We also estimated mean expected H-loss for these species over the next 100 years, and found it to be 9–29%. These estimates of high H-loss and low Ne suggest that some species listed as Endangered likely warrant listing as Critically Endangered if genetic considerations were included. We recommend that RL and other assessment frameworks (i) report methods used for estimating the number of mature adults, (ii) include standardized information on species traits that infu- ence Ne to facilitate Ne estimation, and (iii) consider using concepts like Ne and heterozygosity-loss in risk assessments. Keywords Biodiversity preservation · Conservation genetics · Extinction risk · Efective size · Number of breeders · Population bottleneck Introduction The one process now going on that will take millions of years to correct is the loss of genetic and species Electronic supplementary material The online version of this diversity by the destruction of natural habitats. This is article (https ://doi.org/10.1007/s1059 2-020-01301 -6) contains the folly our descendants are least likely to forgive us. supplementary material, which is available to authorized users. -Edward O. Wilson, 1984 * Brittany A. Garner Biodiversity loss is among the most urgent problems [email protected] facing the world today. The most recognized worldwide Sean Hoban index for biodiversity is the International Union for Con- [email protected] servation of Nature’s (IUCN) Red List. This list results Gordon Luikart from a large, informative, and continually updated database [email protected] dedicated to “providing the world with the most objective, scientifcally-based information on the current status of 1 Interdisciplinary Degree Program and W.A. Franke College of Forestry & Conservation, University of Montana, 32 globally threatened biodiversity” (IUCN 2001). For extant Campus Dr, Missoula, MT 59812, USA organisms with adequate demographic data, the IUCN Red 2 Center for Tree Science, The Morton Arboretum, 4100 List assigns an extinction risk category (“Least Concern”, Illinois Rt 53, Lisle, IL 60532, USA “Near Threatened”, “Vulnerable”, “Endangered”, or “Criti- 3 Flathead Lake Biological Station, Division of Biological cally Endangered”) based upon a variety of criteria (Mace Sciences, University of Montana, 32125 Bio Station Ln, and Lande 1991; IUCN 2001). The IUCN bases most of Polson, MT 59860, USA Vol.:(0123456789)1 3 796 Conservation Genetics (2020) 21:795–801 its risk assessment on factors regarding number of mature (outbred) populations carry a large genetic load (deleterious individuals, trend, and geographic range. The IUCN rec- alleles; Allendorf et al. 2013; Spigler et al. 2017). At small ognizes genetic diversity as one aspect of species diversity and declining Ne, loss of allelic diversity is especially rapid and health (Norse et al. 1986, Reed and Frankham 2003); and increases susceptibility to infectious disease and cancers however, genetic factors are seldom used explicitly in RL (Ujvari et al. 2018). Thus, Ne could inform managers and assessments (Laikre et al. 2009), or in conservation policy other conservation stakeholders about a population’s ability or assessments in general (Pierson et al. 2016). For example, to persist and respond to environmental change, which is of Laikre (2010) concluded that genetic diversity was not moni- great importance in the Anthropocene. tored, genetic change indicators were missing, and no strat- While there are increasingly useful genetic methods to egy had emerged for including genetic aspects into global estimate Ne (e.g., those based on linkage disequilibrium or biodiversity targets, a point reiterated in Laikre et al. 2020. sibship; Waples and Do 2008; Wang et al. 2016; Beaumont Genetic principles and parameters have been useful in and Wang 2019) and genetic data are increasingly aford- assessing conservation priority and risk assessment in a able, Ne need not be empirically measured with molecular range of taxa, particularly when extinction risks are dif- markers for the Ne concept to be useful in assessing risk of fcult to evaluate from ecological and demographic data a species or population. For example, the Ne for a species alone (Dunham et al. 1999). Efective population size (Ne) or taxonomic group is known to often be only 10% to 20% is defned as the size of the ideal population with the same of the Nc (Frankham et al. 2014), and sometimes far less rate of genetic drift as in the actual population being con- (e.g., < 1%; Palstra and Ruzzante 2008). Biologists can esti- sidered (Fisher 1930; Wright 1931). Ne is among the most mate or approximate Ne from Nc using only demographic important genetic parameters in evolutionary and conserva- data such as the number of reproducing males and females, tion biology because it infuences the rate of inbreeding, loss the adult sex ratio, longevity, family size variance, and more of genetic diversity, efciency of natural selection, and the (Waples et al. 2013), if such information is available. This maintenance of evolutionary potential (Newman and Pilson would allow explicit consideration that if Ne ≪ 50 (e.g., 20 to 1997; Waples et al. 2014; Beaumont and Wang 2019). This 30), then inbreeding depression (and fxation of deleterious is in contrast to the population census size, Nc, which is often alleles) and loss of alleles is likely to threaten a population’s defned as the number of mature (adult) individuals (e.g., growth and persistence (Bozzuto et al. 2019). Furthermore, Frankham1995; Waples 2005; Waples et al. 2014). Ne (and Ne estimates allow estimation of the loss of heterozygosity the Ne/Nc ratio) is often particularly small for species with (H-loss) expected over 100 years, for example, if the gen- high fecundity, high mortality in early life stages (type III eration interval is known or approximated. Heterozygosity survivorship), high sex ratio skew, polygamy, and/or herit- loss over 100 years (e.g., > 5% or 10%) has been proposed ability of reproductive success (Waples et al. 2014; Kendall as threshold for population extinction risk and management et al. 2016; Wang 2016; Greenbaum et al. 2017; Sun and concern (e.g., Allendorf and Ryman 2002). Hedgecock 2017). Our overarching goal here is to consider the use of Ne However, the main driver of low Ne and Ne/Nc ratios concepts and estimates, and loss of heterozygosity for IUCN is typically high variation in reproductive success among Red List assessment procedures. Our main objectives are to individuals, which could be due to body size and fecundity (1) assess the standardization of reporting the “number of variation (e.g., large trees or fsh producing thousands of mature individuals” as estimated and reported within the seeds or eggs), behavior (e.g., dominant males; Beletsky and IUCN Red List to facilitate Ne estimation, (2) estimate the Orians 1989), or chance. While some of the extremely low Ne for species listed as endangered (EN) on the IUCN Red Ne/Nc ratios reported in the literature have been contested as List per Criterion D using a range of generally accepted potential artifacts of sampling (Hauser et al. 2002; Ficetola and reasonable Ne/Nc ratios, (3) estimate the heterozygosity et al. 2010; Waples 2016), the ratios in many species are expected to be lost in the next 100 years based on those often small (< 0.10). Ne is often small (< 50) and/or declin- Ne estimations and generation interval estimates, and (4) ing which is problematic for population persistence, and identify which species listed as EN are at the most risk and thus is of concern to conservation biologists (Allendorf and could warrant listing as critically endangered (CR) if the Ryman 2002, Laikre et al. 2020). Ne and heterozygosity-loss are considered. We predict that Ne ranging from around 50 to several hundred is within many species in the IUCN Red List are likely to have a small the range where genetic variation is lost rapidly due to Ne/Nc ratio and Ne < 50 (for multiple generations) and thus genetic drift and deleterious efects of inbreeding likely could beneft from revision of Red List ranking along with occur; Ne below 50 signals critical and rapid genetic ero- monitoring or management actions to prevent excessive loss sion (Frankham et al. 2002; Hoarau et al. 2005). This is of genetic variation and reduced probability of persistence especially true if the population size has been small for (Crow and Kimura 1970; Allendorf and Ryman 2002; Lacy multiple generations and was recently large, because large 2019). 1 3 Conservation Genetics (2020) 21:795–801 797 Methods used for assessments that reported ranges of values for mature individuals.