Within-population genetic diversity underpins wild population resilience and in turn species and ecosystem resilience. The rapidly accelerating biodiversity crisis is motivating the use of both legacy and new datasets, from molecular data and ecological proxies, to inform genetic management and policy. In this Review, we synthesize examples of the integration of genetic principles across data, management and policy scales and illustrate how emerging strategies can halt the erosion of genetic diversity. Biodiversity conservation science increasingly invokes large, heterogeneous, aggregate datasets to identify eco-evolutionary processes that drive change as well as set priorities for policymakers and land managers. Deploying this knowledge to address issues that erode within-population genetic resilience is essential to biodiversity conservation. With careful appreciation of population genetic principles, all available data, from DNA-based studies to ecosystem monitoring, can be recruited towards comprehensive conservation genetics, supporting action across levels of governance. A critical mass of highly diverse datasets and knowledge types is increasingly contributing to legislation, policy and guidelines to monitor genetic processes in nature and, ultimately, protect the richness and resilience of biodiversity. The loss of genetic diversity is a major threat to population resilience, posing a challenge for conservation efforts. This Review highlights how the integration of large-scale biodiversity monitoring datasets and population genetics principles can empower biodiversity partners across governance levels to make effective conservation decisions.
Mitigating loss of genetic diversity is a major global biodiversity challenge1, 2, 3-4. To meet recent international commitments to maintain genetic diversity within species5,6, we need to understand relationships between threats, conservation management and genetic diversity change. Here we conduct a global analysis of genetic diversity change via meta-analysis of all available temporal measures of genetic diversity from more than three decades of research. We show that within-population genetic diversity is being lost over timescales likely to have been impacted by human activities, and that some conservation actions may mitigate this loss. Our dataset includes 628 species (animals, plants, fungi and chromists) across all terrestrial and most marine realms on Earth. Threats impacted two-thirds of the populations that we analysed, and less than half of the populations analysed received conservation management. Genetic diversity loss occurs globally and is a realistic prediction for many species, especially birds and mammals, in the face of threats such as land use change, disease, abiotic natural phenomena and harvesting or harassment. Conservation strategies designed to improve environmental conditions, increase population growth rates and introduce new individuals (for example, restoring connectivity or performing translocations) may maintain or even increase genetic diversity. Our findings underscore the urgent need for active, genetically informed conservation interventions to halt genetic diversity loss.
Mixing gene pools in translocations can create populations with higher genetic diversity and evolutionary potential compared to single sources. However, the benefits of outcrossing on genetic rescue may depend on species' life history, notably mating systems. We assessed outcomes on growth and survival of different kinds of cross in a translocated population of the highly endangered mixed‐mating species Banksia brownii , established from multiple sources. We genetically assigned plants grown from field‐pollinated seed as of selfed, within‐source or between‐source (referring to the original source populations) cross types, and estimated proportion of heterozygous loci for each plant. We modeled the associations among genetic predictors (cross type, level of genetic diversity, and ancestry) and fitness proxies measured in glasshouse and field. At the translocation site, selfing rates were approximately 53–70% and crossing among sources was rare, both likely owing to different patterns of flowering among plants. Offspring of selfed plants were consistently smaller in volume in the glasshouse than were offspring from within‐source crosses. There was no evidence from the first 3 years that survival in the field was influenced by any predictor tested, but the smaller volume of selfed plants in the glasshouse and correlation of glasshouse size at 5 months with the size of the same plants at 3 years in the field suggest that more time may be needed to observe any effects of outcrossing on survival and fitness. Our results highlight the importance of monitoring mating systems, genetic diversity, and fitness data for evaluating translocation success and informing adaptive management.
Societal Impact Statement Conservation seed banks maintain collections of many seed‐bearing plant species, providing germplasm and data to support management of wild populations. However, a proportion of plant species produce seeds that are difficult to collect, dry, store and utilise; these are known as ‘exceptional’ species. Here we tested a framework for identifying exceptional species, to document examples and provide case studies within the Australian flora. We present a workflow that may be used to identify additional exceptional species, and direct efforts to establish appropriate collection types (seeds and/or living collections, tissue culture or cryopreservation) for their ex situ conservation. Summary Seed banking is well established to contribute to the conservation of many seed‐bearing plant species ex situ for future use in restoration, translocation, agriculture and horticulture. In Australia, over 67% of currently listed threatened plants are represented in conservation seed banks. However, there are challenges to conserving the full extent of plant diversity in seed banks, with growing recognition that we need to think beyond conventional seed banking methods to conserve ‘exceptional’ plant species that are difficult to collect, store and germinate. We examine how the framework for identification of such species can be applied to the Australian flora, using examples from the recently published guidelines for ‘ Plant Germplasm Conservation in Australia ’ and case studies and data arising from the Australian Academy of Science Fenner Conference on the Environment ‘Exceptional Times, Exceptional Plants’ . We present a workflow to assist conservation decision‐makers and practitioners in identifying exceptional species and overcoming barriers to storage of germplasm, enabling appropriate ex situ collection types to be established via seeds, living collections, tissue culture, cryopreservation or a combination of these. Australia's seed conservation sector continues to expand, with increasing expertise, facilities and networks established to conserve a diversity of plant species; however, resolving the challenges relating to each exceptionality factor requires significantly more time, labour and collaboration than current capacity allows. Understanding the barriers to conservation and production of healthy plants, via germination or other methods of propagation, is a critical component of conserving species long‐term and ultimately returning plants to the landscape.
Aim Apomixis is a widespread trait in extreme environments worldwide, yet phylogeographical studies for species exhibiting these complex reproductive systems are still limited to temperate zones in the Northern Hemisphere. Through analyses of a combination of adult plants and seedlings, and nuclear and chloroplast DNA, we assessed the contemporary genetic outcomes of apomixis and phylogeographical patterns in an arid unglaciated landscape to understand the evolutionary trajectory of apomictic species.Location Pilbara bioregion, north-western Australia.Taxon Senna glutinosa subsp. glutinosa.Materials and MethodsSpatial patterns of genetic diversity and differentiation in three chloroplast regions and 17 nuclear microsatellite markers were evaluated in 480 plants from 20 populations of S. glutinosa subsp. glutinosa across the Pilbara bioregion. We also germinated and genotyped seed for a progeny analysis to quantify polyembryony and the relative frequency of asexual versus sexual reproduction.Results We found frequent polyembryony and a high proportion of asexual offspring (84.56%), resulting in low within-population genotypic diversity. The nuclear dataset identified 72 multilocus lineages (MLLs) with moderate pairwise population genetic fixation and low differentiation among populations with no geographically structured genetic clustering. Chloroplast DNA showed high haplotype diversity and a widespread distribution of haplotypes. Only one peripheral population presented a single unique haplotype and MLL.Main Conclusions Analysis of this woody perennial in an arid landscape shows the influence of apomixis on genetic patterns and species persistence. Haplotype diversity was indicative of long-term persistence within the ancient Pilbara region. Widespread distribution of haplotypes and sharing of several nuclear MLLs among distant populations indicated extensive seed dispersal throughout the study area. The combination of polyploidy, facultative apomixis and extensive seed dispersal maintains genetic variability within local populations and promotes the spread of advantageous genotypes across wide geographical distances. Therefore, apomixis, rather than an evolutionary 'dead-end', can be regarded as a mechanism facilitating evolutionary success of apomictic species in extreme and complex environments.
The ultimate goal of threatened plant translocations is to establish self-sustaining populations. Lessons learnt from plant translocations can inform future translocations and improve conservation outcomes via adaptive management. We assessed translocation success for 76 translocations of 50 species established as part of recovery programmes between 1998 and 2016 in the Southwest Australian Floristic Region (SWAFR), a biodiversity hotspot with Mediterranean-type climate. We used a series of Bayesian hierarchical models to assess translocation success as measured by plant survival, height growth, crown growth, and reproduction (flowering and fruiting). We found that fencing to prevent vertebrate herbivory improved survival, irrigating plants over the first two summer dry periods improved the likelihood of reproduction, and where the rainfall increased above the 30-year average in the two years following planting, it positively influenced survival, growth, and reproduction. We recommend that fencing to prevent herbivory should be broadly considered in threatened plant translocations, while irrigation to improve translocation success would benefit plant species in Mediterranean-type ecosystems and other dryland environments.
Context As threatening processes continue to impact rare plant populations, the use of translocations is becoming increasingly frequent. The ultimate success of translocation, attaining long-term persistence, is determined by species’ ability to reproduce, recruit, and maintain levels of genetic diversity that permits the capacity to adapt to environmental change. Aims This study aimed to assess translocation success of Banksia brownii. Methods We compared genetic diversity, reproductive output and aspects of the mating system of a translocated population with four reference wild populations. Key results We found that the use of multiple source populations for the translocation resulted in levels of genetic diversity comparable to reference populations of high diversity. Reproductive output was highest in the translocated population and a positive relationship between plant size and number of flowers across all populations was evident. However, mating system analysis revealed a large difference in outcrossing rates between populations in different habitats despite common pollinators, with the translocated population having the highest rates of selfing. Conclusion Whilst genetic diversity and reproductive output were comparable or higher in the translocated population than in the reference populations, assessing translocation outcomes by these measures alone can potentially mask the longer-term erosion of genetic diversity through unfavourable patterns of mating. Implications We recommend using multiple metrics of reproductive, recruitment and genetic diversity to properly assess plant translocation success.
Taxonomic resolution of infraspecific taxa in Lambertia orbifolia (Proteaceae) using molecular and morphological evidence.Nuytsia 34
A chief tool in plant conservation is the augmenting or establishment of threatened plant populations by translocating individuals grown ex-situ. As translocations become an increasingly common practise in conservation and land management, various techniques to increase survival and persistence have become established as standard. Here we use a large historical database of plant translocations to evaluate the evidence for common management techniques to enhance translocation performance. We found that the most important factors associated with maximising size and survival of translocated plant populations were the number of propagules planted, fencing to protect from herbivores, and stimulating recruitment. Factors influencing the probability of recruitment were less certain, however burning and watering increased its likelihood. We also asked how habitat and lifeform influenced translocation performance. Translocations in grassland habitats performed worse than other habitats, and translocations of their predominant lifeform, the perennial grasses, also compared poorly. Our results make a strong case for the utility of a limited number of management interventions, and we highlight where a more explicit focus on experimental data might build our understanding of the factors influencing success in plant translocations.
Context Empirical studies of intraspecific genetic diversity and population structure can inform the evolutionary and demographic history of individual species and of landscapes at the bioregional level. Aims We aimed to assess intraspecific genetic variation at macroevolutionary and microevolutionary temporal scales for Mirbelia viminalis, a key species present on the Hamersley Range in the ancient and highly diverse landscape of the Pilbara bioregion of northwest Western Australia. Methods We sampled extant populations and assessed diversity and structure using sequences (chloroplast DNA, 1759 base pairs) and microsatellite markers (nuclear DNA, 15 loci) data. Key results Significant phylogeographic structure and a lack of historical demographic signals of population contraction or expansion suggest historical population persistence. Moderate chloroplast haplotype diversity (h = 15) and moderate divergence among extant haplotypes indicates a degree of historical connectivity via seed dispersal across central populations on the Hamersley Range. Levels of nuclear genetic diversity were low to moderate (allelic richness = 3.554, expected heterozygosity = 0.489, observed heterozygosity = 0.462) and depauperate compared to another member of the Mirbelia genus present further south in the Midwest region. Nuclear diversity revealed a strong signal of isolation by distance with localised admixture among populations and some contemporary genetic clustering along a north-west to south-east transect of the Hamersley Range. Conclusions Low nuclear genetic diversity may be related to recent reductions in population size for M. viminalis. Historical population persistence with few barriers to dispersal other than geographic distance may be common for members of the Fabaceae across the Hamersley Range.
Context. To establish translocated populations of threatened plants with the genetic resources to adapt to changing environmental conditions, the source of propagation material is an important consideration. Aim. We investigated the fitness consequences of genetic rescue and admixture for the threatened annual daisy Schoenia filifolia subsp. subulifolia, and the common S. filifolia subsp. filifolia, to inform seed-sourcing strategies for translocations of the threatened subspecies. Methods. We evaluated genetic diversity of two populations of S. filifolia subsp. subulifolia and four populations of S. filifolia subsp. filifolia by using microsatellite markers. We grew seedlings from each study population and cross-pollinated inflorescences within and among populations of the same subspecies, and between subspecies. We evaluated the fitness consequences of each cross by using seed set, seed weight and seed viability. Key results. There was a lower genetic diversity in the small (<50 plants, N-ar = 3.28, H-e = 0.42) compared to the large (>10 000 plants, N-ar = 4.42, H-e = 0.51) population of S. filifolia subsp. subulifolia, although none of the measures was significantly different, and seed fitness was slightly, although not significantly, reduced in interpopulation crosses compared with the small population. Genetic diversity was similar between the threatened and widespread subspecies; however, the subspecies were genetically divergent (F-st = 0.242-0.294) and cross-pollination between subspecies produced negligible amounts of seeds (<3% seed set). Conclusion. Although genetic rescue or admixture of S. filifolia subsp. subulifolia would not necessarily result in greatly increased levels of genetic diversity or seed fitness, we still consider it a potential option. Negligible seed set in crosses between subspecies indicates that deliberate hybridisation is not a possibility.
BACKGROUND AND AIMS:Understanding how genetic diversity is distributed and maintained within species is a central tenet of evolutionary and conservation biology, yet is understudied in arid regions of the globe. In temperate, glaciated environments, high genetic diversity in plant species is frequently found in refugial areas, which are often associated with southern non-glaciated landscapes. In arid, unglaciated environments, landscape features providing mesic conditions are likely to be refugia, although our understanding needs more refinement in these biomes. We test whether refugia and nuclear diversity hotspots occur in high-elevation, topographically complex areas for co-distributed shrubs (Petalostylis labicheoides and Indigofera monophylla; Fabaceae) in the ancient, arid Pilbara bioregion of north-western Australia.METHODS:We conducted extensive sampling of the Pilbara (>1400 individuals from 62 widespread populations) to detect patterns in nuclear diversity and structure based on 13-16 microsatellite loci. Evidence of historical refugia was investigated based on patterns of diversity in three non-coding chloroplast (cp) sequence regions for approx. 240 individuals per species. Haplotype relationships were defined with median-joining networks and maximum likelihood phylogenetic trees.KEY RESULTS:We found cpDNA evidence for a high-elevation refugium in P. labicheoides but not for I. monophylla that instead exhibited extraordinary haplotype diversity and evidence for persistence across a widespread area. Nuclear diversity hotspots occurred in, but were not exclusive to, high-elevation locations and extended to adjacent, low-elevation riparian areas in both species.CONCLUSIONS:Phylogeographic refugia in arid environments may occur in high-elevation areas for some species but not all, and may be influenced by species-specific traits: a mesic montane refugium in P. labicheoides could be related to its preference for growth in water-gaining areas, while a lack of such evidence in I. monophylla could be related to maintenance of cpDNA diversity in a large soil seed bank and dynamic evolutionary history. Mesic environments created by the intersection of topographically complex landscapes with riparian zones can be contemporary reservoirs of genetic diversity in arid landscapes.
Ecological restoration is addressing the challenge of biodiversity conservation in landscapes where native vegetation has been extensively cleared. Reestablishing ecological interactions that support self‐sustainable populations plays an essential role in restoration efforts. For animal‐pollinated plant species, comparing mating system dynamics within restoration populations with natural remnant populations can inform the progress of restoration activities. We assessed mating system parameters, seed weight, invertebrate floral visitors, and genetic diversity for two restoration populations and two native reference remnant populations of the animal‐pollinated, woody shrub/tree, Hakea laurina (Proteaceae) in the Southwest Australian Floristic Region. There was no difference in outcrossing rates between the two sites (restoration and reference populations combined) or treatments (sites combined). However, one restoration population showed significantly lower outcrossing that was correlated with reduced seed weight, greater inbreeding, and significantly lower invertebrate richness and abundance compared to its nearby remnant population. In contrast, in the other restoration population, all measures were comparable to the reference remnant population. Local genetic diversity available in remnant populations was captured in both restoration populations. Limitations to pollinator services may be affecting mating patterns and potentially population fitness, in a younger restoration population with reduced proximity to remnant vegetation, which has a tall coplanted overstorey species and spatially aggregated individuals. We highlight these aspects of restoration populations as important areas of ongoing research that will impact the reestablishment of ecological interactions, and the assessment of mating system dynamics as a valuable tool to inform the current progress of restoration activities.
Context Empirical studies of intraspecific genetic diversity and population structure can inform the evolutionary and demographic history of individual species and of landscapes at the bioregional level. Aims We aimed to assess intraspecific genetic variation at macroevolutionary and microevolutionary temporal scales for Mirbelia viminalis, a key species present on the Hamersley Range in the ancient and highly diverse landscape of the Pilbara bioregion of northwest Western Australia. Methods We sampled extant populations and assessed diversity and structure using sequences (chloroplast DNA, 1759 base pairs) and microsatellite markers (nuclear DNA, 15 loci) data. Key results Significant phylogeographic structure and a lack of historical demographic signals of population contraction or expansion suggest historical population persistence. Moderate chloroplast haplotype diversity (h = 15) and moderate divergence among extant haplotypes indicates a degree of historical connectivity via seed dispersal across central populations on the Hamersley Range. Levels of nuclear genetic diversity were low to moderate (allelic richness = 3.554, expected heterozygosity = 0.489, observed heterozygosity = 0.462) and depauperate compared to another member of the Mirbelia genus present further south in the Midwest region. Nuclear diversity revealed a strong signal of isolation by distance with localised admixture among populations and some contemporary genetic clustering along a north-west to south-east transect of the Hamersley Range. Conclusions Low nuclear genetic diversity may be related to recent reductions in population size for M. viminalis. Historical population persistence with few barriers to dispersal other than geographic distance may be common for members of the Fabaceae across the Hamersley Range.
Context To establish translocated populations of threatened plants with the genetic resources to adapt to changing environmental conditions, the source of propagation material is an important consideration. Aim We investigated the fitness consequences of genetic rescue and admixture for the threatened annual daisy Schoenia filifolia subsp. subulifolia, and the common S. filifolia subsp. filifolia, to inform seed-sourcing strategies for translocations of the threatened subspecies. Methods We evaluated genetic diversity of two populations of S. filifolia subsp. subulifolia and four populations of S. filifolia subsp. filifolia by using microsatellite markers. We grew seedlings from each study population and cross-pollinated inflorescences within and among populations of the same subspecies, and between subspecies. We evaluated the fitness consequences of each cross by using seed set, seed weight and seed viability. Key results There was a lower genetic diversity in the small (<50 plants, Nar = 3.28, He = 0.42) compared to the large (>10 000 plants, Nar = 4.42, He = 0.51) population of S. filifolia subsp. subulifolia, although none of the measures was significantly different, and seed fitness was slightly, although not significantly, reduced in interpopulation crosses compared with the small population. Genetic diversity was similar between the threatened and widespread subspecies; however, the subspecies were genetically divergent (Fst = 0.242–0.294) and cross-pollination between subspecies produced negligible amounts of seeds (<3% seed set). Conclusions Although genetic rescue or admixture of S. filifolia subsp. subulifolia would not necessarily result in greatly increased levels of genetic diversity or seed fitness, we still consider it a potential option. Negligible seed set in crosses between subspecies indicates that deliberate hybridisation is not a possibility. Implications Studies of fitness consequences of admixture or genetic rescue are rare yet critical to assessing the benefits of different translocation strategies.
Topographically heterogeneous areas are likely to act as refugia for species because they facilitate survival during regional climatic stress due to availability of a range of microenvironments. The Stirling Ranges are a topographically complex area in the generally subdued and ancient landscape of south-western Australia. We investigated the influence of these landscape features on the evolutionary history of the rare woody shrub, Banksia brownii through a combined approach using phylogeographic analysis of sequence data from three chloroplast sequences, the trnV–ndhC, trnQ–rps16 , and rpl32–ndhF intergenic spacer regions, and species distribution modeling. The Stirling Ranges showed high genetic diversity and differentiation among populations consistent with localized persistence and maintenance of large populations in an area that species distribution modeling identified as providing habitat stability at the Last Glacial Maximum as well as under warmer conditions. In contrast, populations in the adjacent subdued lowlands showed signals of low diversity, suggesting contraction, and subsequent expansion from localized refugia in the west. Cool summers are an important climatic variable for the species and species distribution modeling showed suitable habitat identified at the LGM suggesting expansion at this time following likely contraction during earlier warmer climatic oscillations. The isolated, coastal population at Vancouver Peninsula showed low diversity but no differentiation and it may have been established in more recent historical times, possibly through Aboriginal movement of seed. Our analysis of B. brownii highlights the complex evolutionary history of the species and the influence of topographic complexity and habitat heterogeneity in this global biodiversity hotspot.
Widespread plant species are expected to maintain genetic diversity and gene flow via pollen and seed dispersal. Stature is a key life history trait that affects seed and potentially pollen dispersal, with limited stature associated with limited dispersal and greater genetic differentiation. We sampled Hill's tabletop wattle (Acacia hilliana) and curry wattle (Acacia spondylophylla), two co-distributed, widespread, Acacia shrubs of low stature, across the arid Pilbara region of north-western Australia. Using chloroplast sequence and nuclear microsatellite data we evaluated patterns of population genetic and phylogeographic diversity and structure, demographic signals, ratios of pollen to seed dispersal, evidence for historical refugia, and association between elevation and diversity. Results showed strong phylogeographic (chloroplast, G(ST) = 0.831 and 0.898 for A. hilliana and A. spondylophylla, respectively) and contemporary (nuclear, F-ST = 0.260 and 0.349 for A. hilliana and A. spondylophylla, respectively) genetic structure in both species. This indicates limited genetic connectivity via seed and pollen dispersal associated with Acacia species of small stature compared to taller tree and shrub acacias across the Pilbara bioregion. This effect of stature on genetic structure is superimposed on moderate levels of genetic diversity that were expected based on widespread ranges (haplotype diversity h = 25 and 12; nuclear diversity He = 0.60 and 0.47 for A. hilliana and A. spondylophylla, respectively). Contemporary genetic structure was congruent at the greater landscape scale, especially in terms of strong genetic differentiation among geographically disjunct populations in less elevated areas. Measures of diversity and connectivity were associated with traits of greater geographic population proximity, population density, population size, and greater individual longevity, and some evidence for range expansion in A. hilliana. Results illustrate that low stature is associated with limited dispersal and greater patterns of genetic differentiation for congenerics in a common landscape and highlight the complex influence of taxon-specific life history and ecological traits to seed and pollen dispersal.