A genetic component of extinction risk in mammals

Over 40% of freshwater fish species in Europe are currently at risk of extinction, highlighting the need for improved conservation planning. This study examines whether the threat status is associated with life-history and ecological traits across 580 autochthonous (native and endemic) freshwater fish species in European inland waters. Using data from FishBase and the IUCN Red List, we assessed associations between threat level and both categorical (e.g., migratory behavior, commercial importance, reproductive guild, and body shape) and numerical traits (e.g., maximum length, weight, age, growth parameters, and maturity traits). Significant, though modest, associations were identified between species threat level and migratory behavior and reproductive guild. Non-migratory species exhibited higher median threat levels, while amphidromous species showed a non-significant trend toward higher threat, suggesting that limited dispersal ability and dependence on fragmented freshwater networks may increase extinction vulnerability. Species with unclassified reproductive strategies also showed elevated threat levels, possibly reflecting both actual risk and underlying data gaps. In contrast, body shape and trophic level were not significantly associated with threat status. Critically Endangered species tend to be larger, heavier, and mature later—traits characteristic of slow life history strategies that limit population recovery. Although length at maturity and maximum age did not differ significantly among IUCN categories, age at maturity was significantly higher in more threatened species, and growth rate (K) was negatively correlated with threat level. Together, these patterns suggest that slower-growing, later-maturing species face elevated extinction risk. Overall, the findings underscore that the threat level in European freshwater fish is shaped by complex interactions between intrinsic biological traits and external pressures. Trait-based approaches can enhance extinction risk assessments and conservation prioritization, especially in data-deficient freshwater ecosystems facing multifaceted environmental challenges.

The ability to undertake torpor has been linked with human‐mediated extinction risk in mammals, but whether torpor serves to elevate or decrease extinction risk, and the mechanism by which it does so, remain controversial. We attempt to clarify the torpor – extinction risk association in a phylogenetic comparative analysis of 284Australian mammal species. We show that the association is strongly mediated by body size. When body mass is included as a covariate, regression models show a negative association between the ability to undertake torpor and current threat status. This association is present in two categories of mammal species likely to be at particular risk from introduced predators (medium‐sized species and species listed as threatened by predation in theInternationalUnion forConservation ofNatureRedList), but there is no association among species not in these categories. This suggests that torpor reduces vulnerability to predators, perhaps by limiting the amount of time spent foraging. However, the association between torpor and extinction risk is also stronger in smaller species, which are more likely to benefit from a reduced energy budget inAustralia's low‐productivity and unpredictable environment. We conclude that the ability to undertake torpor is clearly an advantage to mammal species in coping with human impacts, and that this advantage is conferred through a combination of reduced exposure to predators and reduced energy requirements.

Global climate change is predicted to result in the decline and/or extinction of a large number of animal populations worldwide, and the risk of extinction is likely to be greatest for those species already vulnerable — i.e. those with limited climatic range and/or restricted habitat require- ments. To date, predictive models have failed to take into account the fact that climate change will alter many of the key life history and ecological parameters which determine a species' inherent risk of extinction, such as body mass, size of geographic range and a suite of reproductive traits. Herein, I review contemporary research on the effects of climate change on extinction risk in mammals, focusing on the capacity of climate change to modify those life history traits that inherently alter spe- cies' extinction risk. This review finds strong evidence that climate change has already had marked effects on key life history traits in many mammals. These changes have resulted in both negative and positive effects on reproductive success and adult and offspring survival, with implications for extinc- tion risk in affected species. While the capacity of climate change to alter life history traits in mam- mals is clear, there is currently little research to clarify how these changes have influenced popula- tion growth and dynamics. Other currently overlooked areas of research are also identified.

In writing a review on the role of genetic factors in species' extinction (Jamieson, 2007), I was initially concerned that some would see such an article as a simple re-hash of an old, and perhaps tired, debate (e.g. Caro & Laurenson, 1994; Caughley, 1994; Hedrick et al., 1996). Surely, some might argue, we have moved on from bickering over whether genetic factors such as inbreeding depression can (occasionally) contribute to the processes affecting species' extinction. We have indeed moved on to a point where genetic factors are accepted to have played a pivotal role in the recovery of several different wild populations (Tallmon, Luikart & Waples, 2004; Pimm, Dollar & Bass, 2006). Nevertheless, others have taken the argument even further, where the loss of fitness due to inbreeding depression is seen as an unavoidable consequence of small populations and therefore an undeniable contributor to the increased extinction risk of threatened species (Frankham, Ballou & Briscoe, 2002; Frankham, 2005). At the other extreme, genetic factors apparently do not even warrant a mention in recent studies exploring the correlates of extinction for hundreds of species of island endemics (Blackburn et al., 2004; Duncan & Blackburn, 2004). It was these extremes that were the focal points of my article. I chose to focus on island endemics for two reasons. First, in no other group is the tension between the relative contributions of genetic versus non-genetic factors to extinction risk more evident. This tension boils down to two major consequences of long periods of isolation for island endemics: (1) increased susceptibility to introduced predators (i.e. predator naivety) and (2) lowered genetic diversity and heightened levels of inbreeding. Second, and closer to home, there is a need to understand the relative importance of the widespread occurrence of reduced genetic variation and inbreeding in threatened island endemics in New Zealand (Jamieson, Wallis & Briskie, 2006), where the devastating effects of introduced predators (including humans) are well documented (Worthy & Holdaway, 2002; Wilson, 2004). I associated the two consequences of island isolation – increased susceptibility to predation and increased risk of inbreeding depression – with the primary (but not exclusive) research interests of ecologists versus geneticists, respectively. Reed (2007) argued that dividing conservation biologists into these two camps is part of the problem. Without stating what that problem is, Reed suggested that greater integration of genetic and ecological factors into a single evolutionary framework when dealing with population declines is part of the solution. In fact, all three of the commentaries seem to agree that focusing either on the deterministic drivers of population decline or on the stochastic processes (including genetic effects) that affect populations once they become small should not be seen as competing or opposing approaches to conservation biology. This distinction between deterministic drivers and stochastic processes affecting small populations echoes the earlier debates about the role of genetics in species extinction (e.g. Hedrick et al., 1996). My review merely highlighted the practical problem of distinguishing effects at either end of what is really a continuum, and the relative importance and associated consequences of these extremes for prioritizing conservation resources. Duncan & Blackburn (2007) acknowledge that stochastic factors such as inbreeding could potentially elevate extinction risk, especially in populations on smaller islands, but did not include this possibility in their original analysis (Jamieson, 2007). (Brook et al. (2002) illustrate using population modelling that inbreeding depression alone could shorten the time to extinction by 25–31%, which is not a trivial quantity.) Yet, Duncan & Blackburn (2007) go on to argue that there are several effects other than inbreeding that are predicted to elevate the rate of extinction in small populations, including the likelihood that predators will be able to find and remove every individual. To me, these sound more like competing, rather than complementary explanations for population declines and extinctions. Indeed, Duncan & Blackburn (2007) discount the hypothesis that endemic island species suffer a higher extinction risk because they are more inbred (Frankham, 1998) by showing that the level of endemism is highly correlated with the rates of extinction, which is predicted by the increased susceptibility to exotic predators hypothesis, but not by the inbreeding hypothesis. I believe Frankham (1998, 2005) saw inbreeding depression as playing a direct role in species decline and eventual extinction, a role that Duncan & Blackburn (2007) question when it comes to island endemics. Groombridge (2007) and Reed (2007) agree with Duncan & Blackburn (2007) and Jamieson (2007) that the impact of introduced predators (including humans) was likely so rapid and large as to overwhelm any differences in survival among island endemics due to their level of inbreeding. This conclusion, however, only applies to extinct island endemics. That is why this debate is so important, because the recovery of extant island endemics, which either coexist with introduced predators or are protected from them (e.g. on offshore islands), may be partly or entirely dependent on genetic management. The fact that Duncan & Blackburn (2007) now acknowledge this point is a welcome step forward. Although genetic factors will clearly be relevant in the recovery of some species, my review further argued that Spielman, Brook & Frankham (2004) may have overstated the general role of genetics, and inbreeding in particular, in increasing the risk of extinction for threatened extant species. Reed (2007) makes this argument more forcefully and more convincingly than I did. Reed points to a number of weaknesses with Spielman et al.'s assertion that the majority of threatened species are not driven to extinction before genetic factors impact them, including their assumption of a linear link between reduced fitness and extinction risk. Again, dissecting and debating this point is important. Spielman et al.'s conclusions imply that by demonstrating that a threatened species has reduced genetic variation, it has an immediate increased risk of extinction due to reduced fitness, which Reed (2007) clearly shows is not necessarily the case, especially in the face of significant rates of predation. (There is little argument that reduced genetic diversity could affect the ability of species to adapt to future environment changes, but Spielman et al. (2004) were specifically referring to the short-term and cumulative loss of fitness due to inbreeding and drift.) With the reality of limited resources that most conservation agencies face, it is important to link management actions to the agents of decline and then to prioritize recovery plans accordingly. Simply knowing that a threatened species has low heterozygosity is insufficient evidence by itself to assess either the associated extinction risks or the ability of a species to recover, as noted by Groombridge (2007). In summary, in addition to highlighting the dominant role that human settlement and introduced predators have had in past extinctions of island endemics, Duncan & Blackburn (2007) acknowledge the potential importance that inbreeding could have for the many small and isolated extant populations that have persisted either because of good luck or considerable conservation effort. Groombridge (2007) further acknowledges the need for a better understanding of both ecological and genetic factors as potential drivers of extinction, and how they may differ on a temporal scale. Groombridge (2007) further asks whether New Zealand's primary focus of controlling introduced predators will be sufficient to ensure viable populations in the future. Reed (2007) pleads for a more integrative approach to conservation management whereby the goal should be to maintain populations at sizes that keep the integrity of ecological and evolutionary processes intact. All these are worthwhile take-home messages from this forum. So why has there been so much confusion over the role of genetic factors in the persistence of island endemics? Population viability modelling clearly shows that factors such as inbreeding depression can cause populations to decline to extinction. It is unclear, however, how often such factors exacerbate population declines otherwise caused by ecological or environmental factors. Once the deterministic drivers of population decline are identified and controlled or eliminated, conservation focus should switch to management of population recovery. Perhaps by placing less emphasis on the role that genetic factors have in extinction processes and placing greater focus on their potential role in recovery processes, genetic factors would receive greater attention from biodiversity managers, most of whom (in my experience) have an ecological rather than a genetics background. Of course, the importance of genetic processes will still vary from species to species and our understanding of these processes in wild populations remains incomplete. This generally calls for a plea for further research, but it also highlights the important role that scientific debate has in conservation issues of this nature. I therefore acknowledge the respondents for their critical yet constructive comments, and conclude that the debate over the role of genetic factors in species extinction not only will, but should, continue. I thank the editors for suggesting that my original paper be published as a Featured Paper, and Ian McLean and Jon Waters and Frances Anderson for comments.

Many marine fish species are experiencing population declines, but their extinction risk profiles are largely understudied in comparison to their terrestrial vertebrate counterparts. Selective extinction of marine fish species may result in rapid alteration of the structure and function of ocean ecosystems. In this study, we compiled an ecological trait dataset for 8,185 species of marine ray-finned fishes (class Actinopterygii) from FishBase and used phylogenetic generalized linear models to examine which ecological traits are associated with increased extinction risk, based on the International Union for the Conservation of Nature Red List. We also assessed which threat types may be driving these species toward greater extinction risk and whether threatened species face a greater average number of threat types than non-threatened species. We found that larger body size and/or fishes with life histories involving movement between marine, brackish, and freshwater environments are associated with elevated extinction risk. Commercial harvesting threatens the greatest number of species, followed by pollution, development, and then climate change. We also found that threatened species, on average, face a significantly greater number of threat types than non-threatened species. These results can be used by resource managers to help address the heightened extinction risk patterns we found.

We examined the association between geographic distribution, ecological traits, life history, genetic diversity, and risk of extinction in nonhuman primate species from Costa Rica. All of the current nonhuman primate species from Costa Rica are included in the study; spider monkeys (Ateles geoffroyi), howling monkeys (Alouatta palliata), capuchins (Cebus capucinus), and squirrel monkeys (Saimiri oerstedii). Geographic distribution was characterized accessing existing databases. Data on ecology and life history traits were obtained through a literature review. Genetic diversity was characterized using isozyme electrophoresis. Risk of extinction was assessed from the literature. We found that species differed in all these traits. Using these data, we conducted a Pearson correlation between risk of extinction and ecological and life history traits, and genetic variation, for widely distributed species. We found a negative association between risk of extinction and population birth and growth rates; indicating that slower reproducing species had a greater risk of extinction. We found a positive association between genetic variation and risk of extinction; i.e., species showing higher genetic variation had a greater risk of extinction. The relevance of these traits for conservation efforts is discussed.

Assessing the impact of the Japanese 2005 World Exposition Project on vascular plants’ risk of extinction

Extinction risk varies among species, and comparative analyses can help clarify the causes of this variation. Here we present a phylogenetic comparative analysis of species-level extinction risk across nearly the whole of the class Mammalia. Our aims were to examine systematically the degree to which general predictors of extinction risk can be identified, and to investigate the relative importance of different types of predictors (life history, ecological, human impact and environmental) in determining extinction risk. A single global model explained 27.3% of variation in mammal extinction risk, but explanatory power was lower for region-specific models (median R2=0.248) and usually higher for taxon-specific models (median R2=0.383). Geographical range size, human population density and latitude were the most consistently significant predictors of extinction risk, but otherwise there was little evidence for general, prescriptive indicators of high extinction risk across mammals. Our results therefore support the view that comparative models of relatively narrow taxonomic scope are likely to be the most precise.

Clarifying the emergent fitness associated with sexually selected traits under the current, increasingly anthropogenic selection regimes is important to understand ongoing evolutionary changes in nature and inform the conservation management of endangered species. Several reasons exist why sexual selection may affect extinction risk. Increased risk may result either from inherent trade-offs between sexually selected traits and viability traits or from selective hunting of sexually selected species. Reduced risk is also possible, for instance if the preference for high-performing mates characteristic of sexually selected species has beneficial genetic consequences for the population. Here, I show that the threat level of bovid species increases with large male horn size. This is the first time, to my knowledge, that sexually selected weaponry has been shown to increase extinction risk at the interspecific level. However, threat level was unrelated to another trait under sexual selection, sexual body size dimorphism, indicating that the effect of sexual selection on extinction risk depends on trait-specific interactions with extrinsic factors. The results suggest that the higher threat level of long-horned species is not primarily due to current trophy hunting practices and rather point to environmentally induced viability costs as a possible main driver. Still, the fact that long-horned species are known to be preferred by trophy hunters highlights the importance of continuously monitoring trophy hunting practices to assure their long-term sustainability.

Over 750 native bird species reside in or regularly migrate to Australia, many of which have experienced rapid changes in habitat extent over the past two centuries. By 2020, eight taxa were considered Extinct and 10% threatened with extinction. Understanding the underlying extrinsic and intrinsic factors that increase extinction risk can allow prioritisation of conservation management and research. Here, we use state-of-the-art phylogenetic comparative models to reveal the most important biological traits that predispose Australian bird species to elevated extinction risk. We use an extensive database of their biological traits and relate these to each species’ national and global IUCN extinction risk status as assessed over the past three decades (in 1990, 2000, 2010, and 2020). We show that high evolutionary distinctiveness (uniqueness), island endemism, and an inability to take advantage of agricultural habitats were the most important traits explaining elevated extinction risk in species when phylogeny is controlled for, suggesting that extinction risk is disproportionately high in species with high evolutionary distinctiveness. Extinct taxa were characterised by large body mass and island endemism compared to taxa extant in 2020. Our study provides the largest and most up-to-date analysis of the intrinsic traits of Australian birds in relation to their extinction risk, and can be used as a baseline in future studies, for prioritisation of conservation actions, and for policy advice on a broad scale.

Phylogenetic information is becoming a recognized basis for evaluating conservation priorities, but associations between extinction risk and properties of a phylogeny such as diversification rates and phylogenetic lineage ages remain unclear. Limited taxon-specific analyses suggest that species in older lineages are at greater risk. We calculate quantitative properties of the mammalian phylogeny and model extinction risk as an ordinal index based on International Union for Conservation of Nature Red List categories. We test for associations between lineage age, clade size, evolutionary distinctiveness and extinction risk for 3308 species of terrestrial mammals. We show no significant global or regional associations, and three significant relationships within taxonomic groups. Extinction risk increases for evolutionarily distinctive primates and decreases with lineage age when lemurs are excluded. Lagomorph species (rabbits, hares and pikas) that have more close relatives are less threatened. We examine the relationship between net diversification rates and extinction risk for 173 genera and find no pattern. We conclude that despite being under-represented in the frequency distribution of lineage ages, species in older, slower evolving and distinct lineages are not more threatened or extinction-prone. Their extinction, however, would represent a disproportionate loss of unique evolutionary history.

A recent complete assessment of the conservation status of 5487 mammal species demonstrated that at least one-fifth are at risk of extinction in the wild. We retrospectively identified genuine changes in extinction risk for mammals between 1996 and 2008 to calculate changes in the International Union for Conservation of Nature (IUCN) Red List Index (RLI). Species-level trends in the conservation status of mammalian diversity reveal that extinction risk in large-bodied species is increasing, and that the rate of deterioration has been most accelerated in the Indomalayan and Australasian realms. Expanding agriculture and hunting have been the main drivers of increased extinction risk in mammals. Site-based protection and management, legislation, and captive-breeding and reintroduction programmes have led to improvements in 24 species. We contextualize these changes, and explain why both deteriorations and improvements may be under-reported. Although this study highlights where conservation actions are leading to improvements, it fails to account for instances where conservation has prevented further deteriorations in the status of the world's mammals. The continued utility of the RLI is dependent on sustained investment to ensure repeated assessments of mammals over time and to facilitate future calculations of the RLI and measurement against global targets.

Biodiversity indices often combine data from different species when used in monitoring programs. Heuristic properties can suggest preferred indices, but we lack objective ways to discriminate between indices with similar heuristics. Biodiversity indices can be evaluated by determining how well they reflect management objectives that a monitoring program aims to support. For example, the Convention on Biological Diversity requires reporting about extinction rates, so simple indices that reflect extinction risk would be valuable. We developed 3 biodiversity indices that are based on simple models of population viability that relate extinction risk to abundance. We based the first index on the geometric mean abundance of species and the second on a more general power mean. In a third index, we integrated the geometric mean abundance and trend. These indices require the same data as previous indices, but they also relate directly to extinction risk. Field data for butterflies and woodland plants and experimental studies of protozoan communities show that the indices correlate with local extinction rates. Applying the index based on the geometric mean to global data on changes in avian abundance suggested that the average extinction probability of birds has increased approximately 1% from 1970 to 2009.Conectando Índices para el Monitoreo de la Biodiversidad con la Teoría de Riesgo de ExtinciónResumenLos índices de biodiversidad combinan frecuentemente los datos de diferentes especies cuando se usan en los programas de monitoreo. Las propiedades heurísticas pueden sugerir índices preferidos, pero carecemos de medios objetivos para discriminar a los índices con propiedades heurísticas similares. Los índices de biodiversidad pueden evaluarse al determinar qué tan bien reflejan los objetivos de manejo que un programa de monitoreo busca apoyar. Por ejemplo, la Convención sobre la Diversidad Biológica requiere reportar las tasas de extinción, así que los índices que reflejan el riesgo de extinción serían valiosos. Desarrollamos 3 índices de biodiversidad que se basan en modelos sencillos de viabilidad de población y que relacionan el riesgo de extinción con la abundancia. Basamos el primer índice en la media geométrica de la abundancia de especies, y el segundo en una media de poder más general. En el tercer índice integramos la media geométrica y la tendencia. Estos índices requieren los mismos datos que índices previos, pero también se relacionan directamente con el riesgo de extinción. La información de campo sobre mariposas y plantas de bosque, y los estudios experimentales de comunidades protozoarias, muestran que los índices se correlacionan con las tasas locales de extinción. Al aplicar el índice basado en la media geométrica sobre los datos globales de los cambios en la abundancia de aves, sugirió que la probabilidad de extinción promedio de aves ha incrementado aproximadamente 1% desde 1970 hasta 2009.Palabras ClaveÍndice de biodiversidad, media geométrica, medida de la biodiversidad, riesgo de extinción

Genetics and extinction

news and update ISSN 1948-6596 commentary Monotypic species and extinction risk: looking at lagomorphs Innovative perspectives in meta-analyses, like the study of lagomorph diversity produced by Verde Arregoitia et al. (2013), are clarifying the poorly understood relationship between biodiversity and ecosystem function. As a result, maintaining cur- rent ecosystem function relies on the preservation of as much biodiversity as possible, especially for rare or unusual clades that may have specialized roles in their environments. Species-poor verte- brate clades are more common than predicted to occur by chance (Ricklefs et al. 2007), suggesting that non-random mechanisms promote the persis- tence of relict species, members of once-large clades that rarely generate new species (Fig. 1). These species-poor clades, which have low net diversification, are thought to be at greater extinc- tion risk in the anthropogenic world because of their propensity to contain species with marginal, specialized niches (Verde Arregoitia et al. 2015; Ricklefs et al. 2007). Loss of these clades would disproportionately impact global biodiversity, due to their evolutionary uniqueness, and potentially ecosystem function if evolutionary uniqueness is also related to both unusual and important func- tional characteristics (Hampe and Petit 2005). In Lagomorpha, unlike other mammalian orders (such as Rodentia), there is a direct correla- tion between genus size and extinction risk, where species-poor clades are more likely to include threatened species (Verde Arregoitia et al. 2013). This correlation may explain why an unusually high proportion of lagomorphs overall is under threat of extinction. In a follow-up study, Verde Arregoitia et al. (2015) seek to explain the poten- tial underlying causes of this pattern. They find that lagomorph diversity tends to be low in bioti- cally diverse areas like the tropics, and high in are- as with low richness of other mammal species. They find that lagomorphs are most diverse in temperate latitudes, opposing the latitudinal di- versity gradient that predominates in most taxa. Sensitivity to high temperatures restricts the geo- graphic ranges of many of these species (Rolland et al. 2014). Verde Arregoitia et al. (2015) also find that evolutionary distinctiveness does not corre- late with biogeographic patterns like range size. These counterintuitive results may also have im- plications for niche breadth, which is often related to range size. Classic ecological studies of species and their habitats offer snapshots of species’ current niches. However, they may not provide broad- enough information about a species’ extinction risk or whether relatives should be expected to share similar risks. In conjunction with fossils and paleoenvironmental data, phylogenetics can be used to reconstruct within-clade evolutionary re- lationships, providing historical and evolutionary insight into potential threats (Cavender-Bares et al. 2012). Measures of extinction risk can often be informed by study of processes that have driven extinction in a clade in the past or through analy- sis of risk to related species by highlighting ecolog- ical, biogeographic, and evolutionary similarities and differences between family members (Ricklefs Contrary to expectations, Verde Arregoitia et al. (2015) found that there may not be a direct relationship between evolutionary distance and extinction risk for species-poor lagomorph genera. Rather (p.9), “...threatened and species-poor gen- era... occur in productive megadiverse areas that currently experience strong habitat degrada- tion...” and increasing anthropogenic pressure, whereas species in more diverse genera tend to live in harsher environments that have much low- er overall mammalian diversity. Thus, the correla- tion between genus size and extinction risk is driv- en by a relationship between genus size and habi- tat quality, in which high-productivity and at-risk habitats contain a disproportionately large num- ber of species-poor lagomorph genera. Further work is necessary to determine whether this rela- tionship is due to lagomorphs’ ability to exploit nutrient-poor habitats (Hirakawa 2002 Hacklander et al. 2008), or due to neutral processes. This relationship between genus size and habitat quality contradicts a common explanation frontiers of biogeography 7.2, 2015 — © 2015 the authors; journal compilation © 2015 The International Biogeography Society