Genetic diversity goals and targets have improved, but remain insufficient for clear implementation of the post-2020 global biodiversity framework.

Genetic diversity among and within populations of all species is necessary for people and nature to survive and thrive in a changing world. Over the past three years, commitments for conserving genetic diversity have become more ambitious and specific under the Convention on Biological Diversity's (CBD) draft post-2020 global biodiversity framework (GBF). This Perspective article comments on how goals and targets of the GBF have evolved, the improvements that are still needed, lessons learned from this process, and connections between goals and targets and the actions and reporting that will be needed to maintain, protect, manage and monitor genetic diversity. It is possible and necessary that the GBF strives to maintain genetic diversity within and among populations of all species, to restore genetic connectivity, and to develop national genetic conservation strategies, and to report on these using proposed, feasible indicators.

Modeling genetic benefits and financial costs of integrating biobanking into the conservation breeding of managed marsupials.

Managed breeding programs are an important tool in marsupial conservation efforts but may be costly and have adverse genetic effects in unavoidably small captive colonies. Biobanking and assisted reproductive technologies (ARTs) could help overcome these challenges, but further demonstration of their potential is required to improve uptake. We used genetic and economic models to examine whether supplementing hypothetical captive populations of dibblers (Parantechinus apicalis) and numbats (Myrmecobius fasciatus) with biobanked founder sperm through ARTs could reduce inbreeding, lower required colony sizes, and reduce program costs. We also asked practitioners of the black-footed ferret (Mustela nigripes) captive recovery program to complete a questionnaire to examine the resources and model species research pathways required to develop an optimized biobanking protocol in the black-footed ferret. We used data from this questionnaire to devise similar costed research pathways for Australian marsupials. With biobanking and assisted reproduction, inbreeding was reduced on average by between 80% and 98%, colony sizes were on average 99% smaller, and program costs were 69- to 83-fold lower. Integrating biobanking made long-standing captive genetic retention targets possible in marsupials (90% source population heterozygosity for a minimum of 100 years) within realistic cost frameworks. Lessons from the use of biobanking technology that contributed to the recovery of the black-footed ferret include the importance of adequate research funding (US$4.2 million), extensive partnerships that provide access to facilities and equipment, colony animals, appropriate research model species, and professional and technical staff required to address knowledge gaps to deliver an optimized biobanking protocol. Applied research investment of A$133 million across marsupial research pathways could deliver biobanking protocols for 15 of Australia's most at-risk marsupial species and 7 model species. The technical expertise and ex situ facilities exist to emulate the success of the black-footed ferret recovery program in threatened marsupials using these research pathways. All that is needed now for significant and cost-effective conservation gains is greater investment by policy makers in marsupial ARTs.

Los programas de reproducción controlada son una herramienta importante para los esfuerzos de conservación de marsupiales, aunque pueden resultar costosos y tener efectos genéticos adversos en las colonias cautivas incapaces de aumentar en tamaño. Los biobancos y las tecnologías de reproducción asistida (TRA) podrían ayudar a superar estos problemas, pero es necesario seguir demostrando su potencial para mejorar su adopción. Utilizamos modelos genéticos y económicos para analizar si la introducción de esperma fundador proveniente de biobancos mediante tecnologías de reproducción asistida a poblaciones cautivas hipotéticas de los marsupiales Parantechinus apicalis y Myrmecobius fasciatus podría reducir la endogamia, disminuir el tamaño efectivo de las colonias y reducir el costo de los programas. También pedimos a los profesionales del programa de recuperación en cautiverio del hurón de patas negras (Mustella nigripes) que respondieran un cuestionario para analizar los recursos y los métodos de investigación de las especies modelo necesarias para desarrollar un protocolo de biobanco optimizado para el hurón de patas negras. Utilizamos los datos de este cuestionario para diseñar métodos de investigación con costos similares para los marsupiales australianos. Con el biobanco y la reproducción asistida, la endogamia se redujo en promedio entre un 80 y un 98%, el tamaño de las colonias fue en promedio un 99% más pequeño y los costos del programa entre 69 y 83 veces menores. La integración del biobanco posibilitó los objetivos de retención genética en cautiverio a largo plazo en marsupiales (90% de heterocigosidad de la población de origen durante un mínimo de 100 años) dentro de un marco realista de costos. Entre el aprendizaje extraído del uso de la tecnología de biobancos que contribuyó a la recuperación del hurón de patas negras figuran la importancia de una financiación adecuada de la investigación (4.2 millones de dólares), colaboraciones profundas que faciliten el acceso a instalaciones y equipos, colonias de animales, especies modelo adecuadas para la investigación y el personal profesional y técnico necesario para abordar las lagunas de conocimiento y ofrecer un protocolo optimizado para los biobancos. Una inversión en investigación aplicada de 133 millones de dólares australianos para la investigación de los marsupiales podría proporcionar protocolos de biobancos para 15 de las especies de marsupiales australianos en mayor riesgo y 7 especies modelo. Existen los conocimientos técnicos y las instalaciones ex situ para emular el éxito del programa de recuperación del hurón de patas negras en marsupiales amenazados utilizando estas vías de investigación. Ahora sólo se necesita una mayor inversión por parte de los responsables políticos de las TRA para marsupiales para obtener beneficios de conservación significativos y rentables.

Modelling Genetic Benefits and Financial Costs of Integrating Biobanking into the Captive Management of Koalas.

Zoo and wildlife hospital networks are set to become a vital component of Australia's contemporary efforts to conserve the iconic and imperiled koala (Phascolarctos cinereus). Managed breeding programs held across zoo-based networks typically face high economic costs and can be at risk of adverse genetic effects typical of unavoidably small captive colonies. Emerging evidence suggests that biobanking and associated assisted reproductive technologies could address these economic and genetic challenges. We present a modelled scenario, supported by detailed costings, where these technologies are optimized and could be integrated into conservation breeding programs of koalas across the established zoo and wildlife hospital network. Genetic and economic modelling comparing closed captive koala populations suggest that supplementing them with cryopreserved founder sperm using artificial insemination or intracytoplasmic sperm injection could substantially reduce inbreeding, lower the required colony sizes of conservation breeding programs, and greatly reduce program costs. Ambitious genetic retention targets (maintaining 90%, 95% and 99% of source population heterozygosity for 100 years) could be possible within realistic cost frameworks, with output koalas suited for wild release. Integrating biobanking into the zoo and wildlife hospital network presents a cost-effective and financially feasible model for the uptake of these tools due to the technical and research expertise, captive koala colonies, and ex situ facilities that already exist across these networks.

Integrating biobanking could produce significant cost benefits and minimise inbreeding for Australian amphibian captive breeding programs.

Captive breeding is an important tool for amphibian conservation despite high economic costs and deleterious genetic effects of sustained captivity and unavoidably small colony sizes. Integration of biobanking and assisted reproductive technologies (ARTs) could provide solutions to these challenges, but is rarely used due to lack of recognition of the potential benefits and clear policy direction. Here we present compelling genetic and economic arguments to integrate biobanking and ARTs into captive breeding programs using modelled captive populations of two Australian threatened frogs, namely the orange-bellied frog Geocrinia vitellina and the white bellied frog Geocrinia alba . Back-crossing with frozen founder spermatozoa using ARTs every generation minimises rates of inbreeding and provides considerable reductions in colony size and program costs compared with conventional captive management. Biobanking could allow captive institutions to meet or exceed longstanding genetic retention targets (90% of source population heterozygosity over 100 years). We provide a broad policy direction that could make biobanking technology a practical reality across Australia's ex situ management of amphibians in current and future holdings. Incorporating biobanking technology widely across this network could deliver outcomes by maintaining high levels of source population genetic diversity and freeing economic resources to develop ex situ programs for a greater number of threatened amphibian species.

Rapid reshaping: the evolution of morphological changes in an introduced beach daisy.

Thousands of species have been introduced to new ranges worldwide. These introductions provide opportunities for researchers to study evolutionary changes in form and function in response to new environmental conditions. However, almost all previous studies of morphological change in introduced species have compared introduced populations to populations from across the species' native range, so variation within native ranges probably confounds estimates of evolutionary change. In this study, we used microsatellites to locate the source population for the beach daisy Arctotheca populifolia that had been introduced to eastern Australia. We then compared four introduced populations from Australia with their original South African source population in a common-environment experiment. Despite being separated for less than 100 years, source and introduced populations of A. populifolia display substantial heritable morphological differences. Contrary to the evolution of increased competitive ability hypothesis, introduced plants were shorter than source plants, and introduced and source plants did not differ in total biomass. Contrary to predictions based on higher rainfall in the introduced range, introduced plants had smaller, thicker leaves than source plants. Finally, while source plants develop lobed adult leaves, introduced plants retain their spathulate juvenile leaf shape into adulthood. These changes indicate that rapid evolution in introduced species happens, but not always in the direction predicted by theory.

Conservation and Genetics.

Humans are responsible for a cataclysm of species extinction that will change the world as we see it, and will adversely affect human health and wellbeing. We need to understand at individual and societal levels why species conservation is important. Accepting the premise that species have value, we need to next consider the mechanisms underlying species extinction and what we can do to reverse the process. One of the last stages of species extinction is the reduction of a species to a few populations of relatively few individuals, a scenario that leads invariably to inbreeding and its adverse consequences, inbreeding depression. Inbreeding depression can be so severe that populations become at risk of extinction not only because of the expression of harmful recessive alleles (alleles having no phenotypic effect when in the heterozygous condition, e.g., Aa, where a is the recessive allele), but also because of their inability to respond genetically with sufficient speed to adapt to changing environmental conditions. However, new conservation approaches based on foundational quantitative and population genetic theory advocate for active genetic management of fragmented populations by facilitating gene movements between populations, i.e., admixture, or genetic rescue. Why species conservation is critical, the genetic consequences of small population size that often lead to extinction, and possible solutions to the problem of small population size are discussed and presented.

Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow.

Many species have fragmented distribution with small isolated populations suffering inbreeding depression and/or reduced ability to evolve. Without gene flow from another population within the species (genetic rescue), these populations are likely to be extirpated. However, there have been only ~ 20 published cases of such outcrossing for conservation purposes, probably a very low proportion of populations that would potentially benefit. As one impediment to genetic rescues is the lack of an overview of the magnitude and consistency of genetic rescue effects in wild species, I carried out a meta-analysis. Outcrossing of inbred populations resulted in beneficial effects in 92.9% of 156 cases screened as having a low risk of outbreeding depression. The median increase in composite fitness (combined fecundity and survival) following outcrossing was 148% in stressful environments and 45% in benign ones. Fitness benefits also increased significantly with maternal ΔF (reduction in inbreeding coefficient due to gene flow) and for naturally outbreeding versus inbreeding species. However, benefits did not differ significantly among invertebrates, vertebrates and plants. Evolutionary potential for fitness characters in inbred populations also benefited from gene flow. There are no scientific impediments to the widespread use of outcrossing to genetically rescue inbred populations of naturally outbreeding species, provided potential crosses have a low risk of outbreeding depression. I provide revised guidelines for the management of genetic rescue attempts.

High genetic diversity is not essential for successful introduction.

Some introduced populations thrive and evolve despite the presumed loss of diversity at introduction. We aimed to quantify the amount of genetic diversity retained at introduction in species that have shown evidence of adaptation to their introduced environments. Samples were taken from native and introduced ranges of Arctotheca populifolia and Petrorhagia nanteuilii. Using microsatellite data, we identified the source for each introduction, estimated genetic diversity in native and introduced populations, and calculated the amount of diversity retained in introduced populations. These values were compared to those from a literature review of diversity in native, confamilial populations and to estimates of genetic diversity retained at introduction. Gene diversity in the native range of both species was significantly lower than for confamilials. We found that, on average, introduced populations showing evidence of adaptation to their new environments retained 81% of the genetic diversity from the native range. Introduced populations of P. nanteuilii had higher genetic diversity than found in the native source populations, whereas introduced populations of A. populifolia retained only 14% of its native diversity in one introduction and 1% in another. Our literature review has shown that most introductions demonstrating adaptive ability have lost diversity upon introduction. The two species studied here had exceptionally low native range genetic diversity. Further, the two introductions of A. populifolia represent the largest percentage loss of genetic diversity in a species showing evidence of substantial morphological change in the introduced range. While high genetic diversity may increase the likelihood of invasion success, the species examined here adapted to their new environments with very little neutral genetic diversity. This finding suggests that even introductions founded by small numbers of individuals have the potential to become invasive.

Predicting the probability of outbreeding depression.

Fragmentation of animal and plant populations typically leads to genetic erosion and increased probability of extirpation. Although these effects can usually be reversed by re-establishing gene flow between population fragments, managers sometimes fail to do so due to fears of outbreeding depression (OD). Rapid development of OD is due primarily to adaptive differentiation from selection or fixation of chromosomal variants. Fixed chromosomal variants can be detected empirically. We used an extended form of the breeders' equation to predict the probability of OD due to adaptive differentiation between recently isolated population fragments as a function of intensity of selection, genetic diversity, effective population sizes, and generations of isolation. Empirical data indicated that populations in similar environments had not developed OD even after thousands of generations of isolation. To predict the probability of OD, we developed a decision tree that was based on the four variables from the breeders' equation, taxonomic status, and gene flow within the last 500 years. The predicted probability of OD in crosses between two populations is elevated when the populations have at least one of the following characteristics: are distinct species, have fixed chromosomal differences, exchanged no genes in the last 500 years, or inhabit different environments. Conversely, the predicted probability of OD in crosses between two populations of the same species is low for populations with the same karyotype, isolated for <500 years, and that occupy similar environments. In the former case, we recommend crossing be avoided or tried on a limited, experimental basis. In the latter case, crossing can be carried out with low probability of OD. We used crosses with known results to test the decision tree and found that it correctly identified cases where OD occurred. Current concerns about OD in recently fragmented populations are almost certainly excessive.

Assessing the benefits and risks of translocations in changing environments: a genetic perspective.

Translocations are being increasingly proposed as a way of conserving biodiversity, particularly in the management of threatened and keystone species, with the aims of maintaining biodiversity and ecosystem function under the combined pressures of habitat fragmentation and climate change. Evolutionary genetic considerations should be an important part of translocation strategies, but there is often confusion about concepts and goals. Here, we provide a classification of translocations based on specific genetic goals for both threatened species and ecological restoration, separating targets based on 'genetic rescue' of current population fitness from those focused on maintaining adaptive potential. We then provide a framework for assessing the genetic benefits and risks associated with translocations and provide guidelines for managers focused on conserving biodiversity and evolutionary processes. Case studies are developed to illustrate the framework.

Estimating the potential for adaptation of corals to climate warming.

The persistence of tropical coral reefs is threatened by rapidly increasing climate warming, causing a functional breakdown of the obligate symbiosis between corals and their algal photosymbionts (Symbiodinium) through a process known as coral bleaching. Yet the potential of the coral-algal symbiosis to genetically adapt in an evolutionary sense to warming oceans is unknown. Using a quantitative genetics approach, we estimated the proportion of the variance in thermal tolerance traits that has a genetic basis (i.e. heritability) as a proxy for their adaptive potential in the widespread Indo-Pacific reef-building coral Acropora millepora. We chose two physiologically different populations that associate respectively with one thermo-tolerant (Symbiodinium clade D) and one less tolerant symbiont type (Symbiodinium C2). In both symbiont types, pulse amplitude modulated (PAM) fluorometry and high performance liquid chromatography (HPLC) analysis revealed significant heritabilities for traits related to both photosynthesis and photoprotective pigment profile. However, quantitative real-time polymerase chain reaction (qRT-PCR) assays showed a lack of heritability in both coral host populations for their own expression of fundamental stress genes. Coral colony growth, contributed to by both symbiotic partners, displayed heritability. High heritabilities for functional key traits of algal symbionts, along with their short clonal generation time and high population sizes allow for their rapid thermal adaptation. However, the low overall heritability of coral host traits, along with the corals' long generation time, raise concern about the timely adaptation of the coral-algal symbiosis in the face of continued rapid climate warming.

Genetic adaptation to captivity in species conservation programs.

As wild environments are often inhospitable, many species have to be captive-bred to save them from extinction. In captivity, species adapt genetically to the captive environment and these genetic adaptations are overwhelmingly deleterious when populations are returned to wild environments. I review empirical evidence on (i) the genetic basis of adaptive changes in captivity, (ii) factors affecting the extent of genetic adaptation to captivity, and (iii) means for minimizing its deleterious impacts. Genetic adaptation to captivity is primarily due to rare alleles that in the wild were deleterious and partially recessive. The extent of adaptation to captivity depends upon selection intensity, genetic diversity, effective population size and number of generation in captivity, as predicted by quantitative genetic theory. Minimizing generations in captivity provides a highly effective means for minimizing genetic adaptation to captivity, but is not a practical option for most animal species. Population fragmentation and crossing replicate captive populations provide practical means for minimizing the deleterious effects of genetic adaptation to captivity upon populations reintroduced into the wild. Surprisingly, equalization of family sizes reduces the rate of genetic adaptation, but not the deleterious impacts upon reintroduced populations. Genetic adaptation to captivity is expected to have major effects on reintroduction success for species that have spent many generations in captivity. This issue deserves a much higher priority than it is currently receiving.

Low genetic diversity in the bottlenecked population of endangered non-native banteng in northern Australia.

Undomesticated (wild) banteng are endangered in their native habitats in Southeast Asia. A potential conservation resource for the species is a large, wild population in Garig Gunak Barlu National Park in northern Australia, descended from 20 individuals that were released from a failed British outpost in 1849. Because of the founding bottleneck, we determined the level of genetic diversity in four subpopulations in the national park using 12 microsatellite loci, and compared this to the genetic diversity of domesticated Asian Bali cattle, wild banteng and other cattle species. We also compared the loss of genetic diversity using plausible genetic data coupled to a stochastic Leslie matrix model constructed from existing demographic data. The 53 Australian banteng sampled had average microsatellite heterozygosity (HE) of 28% compared to 67% for outbred Bos taurus and domesticated Bos javanicus populations. The Australian banteng inbreeding coefficient (F) of 0.58 is high compared to other endangered artiodactyl populations. The 95% confidence bounds for measured heterozygosity overlapped with those predicted from our stochastic Leslie matrix population model. Collectively, these results show that Australian banteng have suffered a loss of genetic diversity and are highly inbred because of the initial population bottleneck and subsequent small population sizes. We conclude that the Australian population is an important hedge against the complete loss of wild banteng, and it can augment threatened populations of banteng in their native range. This study indicates the genetic value of small populations of endangered artiodactyls established ex situ.

Comparative losses of quantitative and molecular genetic variation in finite populations of Drosophila melanogaster.

Quantitative genetic variation, the main determinant of the ability to evolve, is expected to be lost in small populations, but there are limited data on the effect, and controversy as to whether it is similar to that for near neutral molecular variation. Genetic variation for abdominal and sternopleural bristle numbers and allozyme heterozygosity were estimated in 23 populations of Drosophila melanogaster maintained at effective population sizes of 25, 50, 100, 250 or 500 for 50 generations, as well as in 19 highly inbred populations and the wild outbred base population. Highly significant negative regressions of proportion of initial genetic variation retained on inbreeding due to finite population size were observed for both quantitative characters (b = -0.67 +/- 0.14 and -0.58 +/- 0.11) and allozyme heterozygosity (b = -0.79 +/- 0.10), and the regression coefficients did not differ significantly. Thus, quantitative genetic variation is being lost at a similar rate to molecular genetic variation. However, genetic variation for all traits was lost at rates significantly slower than predicted by neutral theory, most likely due to associative overdominance. Positive, but relatively low correlations were found among the different measures of genetic variation, but their low magnitudes were attributed to large sampling errors, rather than differences in the underlying processes of loss.

Most species are not driven to extinction before genetic factors impact them.

There is controversy concerning the role of genetic factors in species extinctions. Many authors have asserted that species are usually driven to extinction before genetic factors have time to impact them, but few studies have seriously addressed this issue. If this assertion is true, there will be little difference in genetic diversity between threatened and taxonomically related nonthreatened species. We compared average heterozygosities in 170 threatened taxa with those in taxonomically related nonthreatened taxa in a comprehensive metaanalysis. Heterozygosity was lower in threatened taxa in 77% of comparisons, a highly significant departure from the predictions of the no genetic impact hypothesis. Heterozygosity was on average 35% lower (median 40%) in threatened taxa than in related nonthreatened ones. These differences in heterozygosity indicate lowered evolutionary potential, compromised reproductive fitness, and elevated extinction risk in the wild. Independent evidence from stochastic computer projections has demonstrated that inbreeding depression elevates extinction risk for threatened species in natural habitats when all other threatening processes are included in the models. Thus, most taxa are not driven to extinction before genetic factors affect them adversely.

Genetics and conservation biology.

Conservation genetics encompasses genetic management of small populations, resolution of taxonomic uncertainties and management units, and the use of molecular genetic analyses in forensics and to understanding species' biology. The role of genetic factors in extinctions of wild populations has been controversial, but evidence now shows that they make important contributions to extinction risk. Inbreeding has been shown to cause extinctions of wild populations, computer projections indicate that inbreeding depression has important effects on extinction risk, and most threatened species show signs of genetic deterioration. Inappropriate management is likely to result if genetic factors are ignored in threatened species management.

Fitness and adaptation in a novel environment: effect of inbreeding, prior environment, and lineage.

The ability of populations to undergo adaptive evolution depends on the presence of genetic variation for ecologically important traits. The maintenance of genetic variation may be influenced by many variables, particularly long-term effective population size and the strength and form of selection. The roles of these factors are controversial and there is very little information on their impacts for quantitative characters. The aims of this study were to determine the impacts of population size and variable versus constant prior environmental conditions on fitness and the magnitude of response to selection. Outbred and inbred populations of Drosophila melanogaster were maintained under benign, constant stressful, and variably stressful conditions for seven generations, and then forced to adapt to a novel stress for seven generations. Fitness and adaptability were assayed in each replicate population. Our findings are that: (1) populations inbred in a variable environment were more adaptable than those inbred in a constant environment; (2) populations adapted to a prior stressful environment had greater fitness when reared in a novel stress than those less adapted to stress; (3) inbred populations had lower fitness and were less adaptable than the outbred population they were derived from; and (4) strong lineage effects were detectable across environments in the inbred populations.