Adaptive evolutionary conservation: towards a unified concept for defining conservation units

Recent years have seen a debate over various methods that could objectively prioritize conservation value below the species level. Most prominent among these has been the evolutionarily significant unit (ESU). We reviewed ESU concepts with the aim of proposing a more unified concept that would reconcile opposing views. Like species concepts, conflicting ESU concepts are all essentially aiming to define the same thing: segments of species whose divergence can be measured or evaluated by putting differential emphasis on the role of evolutionary forces at varied temporal scales. Thus, differences between ESU concepts lie more in the criteria used to define the ESUs themselves rather than in their fundamental essence. We provide a context-based framework for delineating ESUs which circumvents much of this situation. Rather than embroil in a befuddled debate over an optimal criterion, the key to a solution is accepting that differing criteria will work more dynamically than others and can be used alone or in combination depending on the situation. These assertions constitute the impetus behind adaptive evolutionary conservation.     

Cryptic divergent lineages of Pultenaea pauciflora M.B. Scott (Fabaceae: Mirbelieae) exhibit different evolutionary history

Genetic structure among disjunct population groups of Pultenaea pauciflora was assessed to determine the evolutionary history of this species as a basis for conservation management strategies. Analysis of individuals from all extant populations using 1737 amplified length polymorphism markers revealed two highly divergent genetic entities with strong geographical structuring. Populations located at Narrogin and Brookton clustered together in Bayesian assignment analysis with every individual optimally placed in a single cluster with complete membership. Genetic differentiation between populations in these two areas was very low. Populations at Boddington were highly divergent from those located at Narrogin and Brookton. All individuals from Boddington populations were optimally placed into a second cluster with complete membership. Populations located at Boddington maintain lower levels of allelic diversity, yet greater levels of mean heterozygosity than populations located at Narrogin and Brookton. The degree of genetic differentiation and different patterns of genetic diversity strongly suggest historical divergence and separate evolutionary influences on the two lineages that occur in different ecological habitat. These Evolutionary Significant Units are likely to represent two cryptic sister taxa in the extant populations currently recognized as P. pauciflora, and the reassessment of taxonomic and conservation status of both lineages is required. © 2013 State of Western Australia. Biological Journal of the Linnean Society © 2013 The Linnean Society of London     

线粒体DNA（mtDNA）多态性在动物保护生物学中的应用

本文从两个方面论述了mtDNA在动物保护生物学中的应用：一是对物种进行遗传多样性的检 测与管理,二是进行与种群统计学数据相关的遗传分析。前者与保护的长期效益（如进化） 密切相关,而后者则主要用于指导短期管理措施的制定。同时,本文重点论述了mtDNA在进 化显著单位(ESUs)和管理单位(MUs)的认定方面的作用。认定ESUs的目的是隔离管理遗传多 样性,它是一系列系统进化史独特的种群,这种独特性同时表现在mtDNA和核DNA上;MUs是 种群统计意义上的生殖隔离单位,具有独特的等位基因频率,与系统发生结构和遗传分歧水 平无关。ESUs与MUs都是保护生物学中保护与管理的重要基本单位。     

分子系统学在生物保护中的意义

本文综述了近年来分子系统学的原理和方法及其在生物多样性保护中的应用和发展。分子系统学方法可以很好地确定物种保护的基本单元——进化显著性单元,并可用于推测群体的发展状态,从而为物种的保护提供了一项新的具很强操作性的科学手段。     

Population structure of North American beluga whales (Delphinapterus leucas) based on nuclear DNA microsatellite variation and contrasted with the population structure revealed by mitochondrial DNA variation

Beluga whales ( Delphinapterus leucas ) in North American waters migrate seasonally between wintering areas in broken pack ice and summering locations in estuaries and other open water areas in the Arctic and sub-Arctic. Results from our previous investigation of beluga whale mitochondrial DNA (mtDNA) revealed genetic heterogeneity among beluga from different summering locations that was interpreted as representing a high degree of summering site philopatry. However, mtDNA is maternally inherited and does not reflect mating that may occur among beluga from different summering locations in wintering areas or during annual migrations. To test the possibility that breeding occurs among beluga from different summering locations, genetic variability at five nuclear DNA (nDNA) microsatellite loci was examined in the same animals tested in the mtDNA study. Beluga samples ( n = 640) were collected between 1984 and 1994 from 24 sites across North America, mostly during the summer. Whales from the various sites were categorized into eight summering locations as identified by mtDNA analysis, as well as four hypothesized wintering areas: Bering Sea, Hudson Strait (Hudson Strait, Labrador Sea, southwest Davis Strait), Baffin Bay (North Water, east Davis Strait), and St Lawrence River. Microsatellite allele frequencies indicated genetic homogeneity among animals from summering sites believed to winter together but differentiation among whales from some of the wintering areas. In particular, beluga from western North America (Bering Sea) were clearly distinguished from beluga from eastern North America (Hudson Strait, Baffin Bay, and St Lawrence River). Based upon the combined data set, the population of North American beluga whales was divided into two evolutionarily significant units. However, the population may be further subdivided into management units to reflect distinct groups of beluga at summering locations.     

Population structure of North American beluga whales (Delphinapterus leucas) based on nuclear DNA microsatellite variation and contrasted with the population structure revealed by mitochondrial DNA variation

Beluga whales ( Delphinapterus leucas ) in North American waters migrate seasonally between wintering areas in broken pack ice and summering locations in estuaries and other open water areas in the Arctic and sub-Arctic. Results from our previous investigation of beluga whale mitochondrial DNA (mtDNA) revealed genetic heterogeneity among beluga from different summering locations that was interpreted as representing a high degree of summering site philopatry. However, mtDNA is maternally inherited and does not reflect mating that may occur among beluga from different summering locations in wintering areas or during annual migrations. To test the possibility that breeding occurs among beluga from different summering locations, genetic variability at five nuclear DNA (nDNA) microsatellite loci was examined in the same animals tested in the mtDNA study. Beluga samples ( n = 640) were collected between 1984 and 1994 from 24 sites across North America, mostly during the summer. Whales from the various sites were categorized into eight summering locations as identified by mtDNA analysis, as well as four hypothesized wintering areas: Bering Sea, Hudson Strait (Hudson Strait, Labrador Sea, southwest Davis Strait), Baffin Bay (North Water, east Davis Strait), and St Lawrence River. Microsatellite allele frequencies indicated genetic homogeneity among animals from summering sites believed to winter together but differentiation among whales from some of the wintering areas. In particular, beluga from western North America (Bering Sea) were clearly distinguished from beluga from eastern North America (Hudson Strait, Baffin Bay, and St Lawrence River). Based upon the combined data set, the population of North American beluga whales was divided into two evolutionarily significant units. However, the population may be further subdivided into management units to reflect distinct groups of beluga at summering locations.     

Identifying evolutionarily significant units for conservation of the endangered Malus sieversii using genome‐wide RADseq data

Malus sieversii, a wild progenitor of the domesticated apple, is an endangered species and is assigned second conservation priority by the China Plant Red Data Book. It is urgent to carry out in situ conservation of this species, but previous studies have not identified evolutionarily significant units (ESUs) for conservation management. In this study, we investigated the genetic diversity and relationships of six M. sieversii populations from China using integrated analysis of microsatellite (nSSR) data, genome‐wide SNPs and previous results in order to propose a reasonable conservation management. The results showed that levels of genetic diversity were inconsistently reflected by our nSSR and previous studies, suggesting that indices of genetic diversity are not effective to identify priority conservation areas for M. sieversii. Based on the selection criteria of ESUs for endangered species conservation, ESUs should reflect lineage divergence, geographical separation and different adaptive variation. Our phylogenetic tree based on genome‐wide SNPs yielded a clear relationship of divergent lineages among M. sieversii populations, leading to new different from those of previous studies. Three independent lineages, including the pairs of populations Huocheng‐Yining, Gongliu‐Xinyuan and Tuoli‐Emin, were identified. The geographic distances between populations among the different phylogenetic lineages were much greater than those within the same phylogenetic lineage. A cluster analysis on environmental variables showed that the three independent lineages inhabit different environmental conditions, suggesting that they may have adapted to different environments. Based on the results, we propose that three independent ESUs should be recognized as conservation units for M. sieversii in China.     

Molecular systematics of the Amazonian endemic genus Hylexetastes (Aves: Dendrocolaptidae): taxonomic and conservation implications

Hylexetastes woodcreepers are endemic to the terra firme forests of the Amazon basin. Currently, most taxonomic sources recognize two species of Hylexetastes (H. perrotii and H. stresemanni), each divided into three subspecies. Some authors maintain that the H. perrotii subspecies should be elevated to full species status. In particular, Hylexetastes perrotii brigidai is endemic to the eastern Amazon, the second Amazonian area of endemism (Xingu) most affected by deforestation and habitat degradation. Consequently, the taxonomic status of H. p. brigidai is of particular concern for conservation. Thus far, only morphological characters have been evaluated for the taxonomic delimitation of species and subspecies of Hylexetastes. We present a molecular phylogenetic analysis of all subspecies to help delimit Hylexetastes interspecific limits. Fragments of two mitochondrial (Cytb and ND2) and three nuclear genes (FGB5, G3PDH and MUSK) from 57 Hylexetastes specimens were sequenced. An ecological niche model was estimated to describe more accurately the potential distributions of taxa and to evaluate their vulnerability to ongoing deforestation. Phylogenetic analyses support the paraphyly of the polytypic H. perrotii as currently delimited and the elevation of Hylexetastes perrotii uniformis to full species rank, as well as the presence of three evolutionary significant units (ESUs) within this newly delimited species, including one grouping all H. p. brigidai specimens. Alternatively, under lineage-based species concepts, our results support at least five evolutionary species in Hylexetastes: H. stresemanni, H. undulatus, H. perrotii, H. uniformis and H. brigidai. Each of these taxa and ESUs are distributed in different interfluvial areas of the Amazon basin, which have different degrees of disturbance. Because they occupy the most heavily impacted region among all Hylexetastes ESUs, regular assessments of the conservation statuses of H. p. brigidai and both H. uniformis ESUs are paramount.     

Genetic diversity and structure of the cycad Zamia loddigesii Miq. (Zamiaceae): implications for evolution and conservation

The genetic diversity and structure of four populations of the cycad Zamia loddigesii were studied throughout its range in Mexico. Allozyme electrophoresis of 15 loci was conducted. The mean number of alleles per locus was 1.80 ± 0.09, the percentage of polymorphic loci was 66.6 ± 5.4, and the expected heterozygosity was 0.266 ± 0.02. The results indicated that the genetic diversity was relatively higher, with respect to tropical tree species and other cycads. The genetic variation explained by differences among populations was 18%. On average, gene flow between paired populations was similar ( Nm  = 1.6) to other tropical forest trees and cycad species. Our results indicated that the geographical isolation among populations of Z. loddigesii generated allele loss, as well as a clinal variation in the frequencies of two loci ( MDH and MNR2 ), in relation to the latitudinal distribution of populations. The populations have become fragmented due to increasingly higher pressure of habitat conversion and disturbance. The importance of the establishment of sanctuaries and protected areas and a reduction in deforestation is highlighted in this research as a way of preserving the high genetic diversity of this and other endemic species.  © 2006 The Linnean Society of London, Botanical Journal of the Linnean Society , 2006, 152 , 533–544.     

Australian land snails: a review of ecological research and conservation approaches

Land snails are an important yet often neglected component of Australia's biological diversity. Despite high levels of diversity within this group and the identification of many narrow range endemic species as being of conservation concern, there have been few detailed studies that document the ecology and conservation requirements of the group. A range of threats has been suggested, yet relatively few have been rigorously assessed. Whilst factors such as land clearing are readily apparent and have resulted in extinctions, other threats such as climate change are not well understood. This paper reviews studies conducted on terrestrial molluscs in Australia and highlights the need for further targeted ecological research, given the likely level of on-going threats. We urge researchers to apply rigorous approaches to data collection that will enable a deeper understanding of the factors governing distribution and abundance. Approaches used in other areas of conservation biology offer considerable scope for application to land snails and for the development of appropriate conservation strategies.     

Subpopulations of Cryptocephalus beetles (Coleoptera: Chrysomelidae): geographically close but genetically far

Abstract. The leaf beetles Cryptocephalus coryli, C. decemmaculatus and C. nitidulus are of conservation concern and are included on the UK Biodiversity Action Plan. The distinctiveness of the disjunct remaining populations of these beetles was compared to that of more continuously distributed Cryptocephalus species. This was carried out with a view to defining evolutionary significant units (ESUs) in the rare species. A portion of the cytochrome b gene, an intergenic spacer and partial tRNA was analysed from 93 specimens of Cryptocephalus beetle (Coleoptera: Chrysomelidae). Considerable sequence divergence was apparent in all the species, even at an intersite scale when the distances between sampled localities were very small (< 1 km). Intrapopulation, intersite and interpopulation divergence observed in the rare species was reflected in the species that have a more continuous distribution, implying that dispersal ability in these species is poor and gene flow can be impeded by relatively trivial barriers to dispersal. The evidence suggests that the disjunct populations of the rare Cryptocephalus species can, tentatively, be considered as ESUs. This has important implications for management strategies and reintroductions.     

分子标记在濒危物种保护中的应用

分子标记可揭示种群遗传和进化信息, 为制定濒危物种保护措施、指导恢复实践提供重要依据。本文主要介绍了分子标记在濒危物种保护过程不同环节中的应用, 包括: (1)正确识别保护单元, 如排除隐存种和杂交种的影响; (2)确定优先保护单元, 包括优先保护区域、优先保护物种、优先保护种群等; (3)指导迁地保护; (4)对保护工作的动态监测和评估。文章最后探讨了分子标记应用于保护的发展方向, 如开展长期的种群遗传组成监测、切实应用于保护管理实践、将基因组学等遗传信息用于全球变化背景下保护策略的制定等, 期望为分子标记技术在生物多样性保护的研究和实践中提供参考。     

Integrative approaches to guide conservation decisions: Using genomics to define conservation units and functional corridors

Climate change and increasing habitat loss greatly impact species survival, requiring range shifts, phenotypic plasticity and/or evolutionary change for long‐term persistence, which may not readily occur unaided in threatened species. Therefore, defining conservation actions requires a detailed assessment of evolutionary factors. Existing genetic diversity needs to be thoroughly evaluated and spatially mapped to define conservation units (CUs) in an evolutionary context, and we address that here. We also propose a multidisciplinary approach to determine corridors and functional connectivity between CUs by including genetic diversity in the modelling while controlling for isolation by distance and phylogeographic history. We evaluate our approach on a Near Threatened Iberian endemic rodent by analysing genotyping‐by‐sequencing (GBS) genomic data from 107 Cabrera voles (Microtus cabrerae), screening the entire species distribution to define categories of CUs and their connectivity: We defined six management units (MUs) which can be grouped into four evolutionarily significant units (ESUs) and three (putatively) adaptive units (AUs). We demonstrate that the three different categories of CU can be objectively defined using genomic data, and their characteristics and connectivity can inform conservation decision‐making. In particular, we show that connectivity of the Cabrera vole is very limited in eastern Iberia and that the pre‐Pyrenean and part of the Betic geographic nuclei contribute the most to the species genetic diversity. We argue that a multidisciplinary framework for CU definition is essential and that this framework needs a strong evolutionary basis.     

Phylogeographic analysis delimits three evolutionary significant units of least chipmunks in North America and identifies unique genetic diversity within the imperiled Peñasco population

Although least chipmunks (Neotamias minimus) are a widely distributed North American species of least concern, the southernmost population, N. m. atristriatus (Peñasco least chipmunk), is imperiled and a candidate for federal listing as a subspecies. We conducted a phylogeographic analysis across the N. minimus range to assess genomic differentiation and distinctiveness of the N. m. atristriatus population. Additionally, we leveraged the historical component of sampling to conduct a temporal analysis of N. minimus genetic diversity and also considered climate change effects on range persistence probability by projecting a species distribution model into the IPCC5 RCP 2.6 and 8.5 scenarios. We identified three geographically structured groups (West, North, and South) that were supported by both mitochondrial and nuclear data. N. m. atristriatus grouped within a unique South subclade but were not reciprocally monophyletic from N. m. operarius, and nuclear genome analyses did not separate N. m. atristriatus, N. m. caryi, and N. m. operarius. Thus, while least chipmunks in the Southwest represent an evolutionary significant unit, subspecies distinctions were not supported and listing of the Peñasco population as a Distinct Population Segment of N. m. operarius may be warranted. Our results also support consideration of populations with North and West mitogenomes as two additional evolutionary significant units. We found that N. minimus genetic diversity declined by ~87% over the last century, and our models predicted substantial future habitat contraction, including the loss of the full contemporary ranges of N. m. atristriatus, N. m. arizonensis, and N. m. chuskaensis.     

Ancient DNA applications for wildlife conservation

Ancient DNA analyses of historical, archaeological and paleontological remains can contribute important information for the conservation of populations and species that cannot be obtained any other way. In addition to ancient DNA analyses involving a single or few individuals, population level studies are now possible. Biases inherent in estimating population parameters and history from modern genetic diversity are exaggerated when populations are small or have been heavily impacted by recent events, as is common for many endangered species. Going directly back in time to study past populations removes many of the assumptions that undermine conclusions based only on recent populations. Accurate characterization of historic population size, levels of gene flow and relationships with other populations are fundamental to developing appropriate conservation and management plans. The incorporation of ancient DNA into conservation genetics holds a lot of potential, if it is employed responsibly.     

Characteristics and preferences of volunteers in a large national bird conservation program in Australia

Volunteers and citizen scientists can make an important contribution to bird monitoring and threatened species conservation projects. Members of BirdLife Australia’s Threatened Bird Network (TBN), a programme which encouraged community participation in conservation projects for threatened birds, were surveyed in 2013 to gain an insight into their demographics and volunteering motivation and preferences. In the 2013 survey, a large proportion of survey respondents were aged between 55 and 74 years old and over half were retired, representing a higher proportion of retired participants than found in a similar study of TBN members in 2000. A large proportion (69%) of respondents had volunteered with TBN projects (occasionally or at least once per year), despite being involved with other environmental groups. Respondents that volunteered mostly preferred short‐term (one day) field‐based volunteer activities, with nearly half also preferring to travel 50 km or less to participate in a project. Less than one third of respondents had never volunteered with TBN projects; this was attributed to not enough projects close to home, time restrictions and lack of transport. Preferences of volunteers in the 2013 survey were similar to those undertaken in 2000 for the majority of responses, including the preference for the activity occurring outdoors, the importance of regular feedback from the organiser, the moderate importance placed on seeing target species and the lack of importance for the provision of transport. A higher importance was placed on the following factors in the 2013 survey responses compared to 2000 (potentially influenced by the higher number of retirees): Having activities closer to home, the activity not being too physically demanding, the opportunity for free time during the activity, good weather was predicted on the day of the activity, existing skills were adequate for the activity, and accommodation was provided if required.     

A review of applications of environmental DNA for reptile conservation and management

Reptile populations are in decline globally, with total reptile abundance halving in the past half century, and approximately a fifth of species currently threatened with extinction. Research on reptile distributions, population trends, and trophic interactions can greatly improve the accuracy of conservation listings and planning for species recovery, but data deficiency is an impediment for many species. Environmental DNA (eDNA) can detect species and measure community diversity at diverse spatio‐temporal scales, and is especially useful for detection of elusive, cryptic, or rare species, making it potentially very valuable in herpetology. We aim to summarize the utility of eDNA as a tool for informing reptile conservation and management and discuss the benefits and limitations of this approach. A literature review was conducted to collect all studies that used eDNA and focus on reptile ecology, conservation, or management. Results of the literature search are summarized into key discussion points, and the review also draws on eDNA studies from other taxa to highlight methodological challenges and to identify future research directions. eDNA has had limited application to reptiles, relative to other vertebrate groups, and little use in regions with high species richness. eDNA techniques have been more successfully applied to aquatic reptiles than to terrestrial reptiles, and most (64%) of studies focused on aquatic habitats. Two of the four reptilian orders dominate the existing eDNA studies (56% Testudines, 49% Squamata, 5% Crocodilia, 0% Rhynchocephalia). Our review provides direction for the application of eDNA as an emerging tool in reptile ecology and conservation, especially when it can be paired with traditional monitoring approaches. Technologies associated with eDNA are rapidly advancing, and as techniques become more sensitive and accessible, we expect eDNA will be increasingly valuable for addressing key knowledge gaps for reptiles.     

Gene diversity analysis of mitochondrial DNA, microsatellites and allozymes in landlocked Atlantic salmon

This study investigates the patterns of genetic diversity detected in allozymes, mtDNA, and microsatellites, in order to assess their relative efficacy to differentiate sympatric landlocked salmon populations and to estimate changes in genetic diversity between wild and first-generation hatchery fish. Overall, the three genetic markers indicated a genetic differentiation between two sympatric populations of Lake Saint-Jean, Québec. MtDNA and microsatellites also showed significant differences between wild and first-generation hatchery fish originating from the same river. Allozyme analysis was the most limited approach due to the low genetic diversity detected and the necessity to kill specimens. Although low polymorphism was found in mtDNA, it was the most discriminant marker between wild populations. Microsatellite analysis appears to be a promising approach due to its high sensitivity in differentiating wild populations, in detecting changes in allele composition between wild and first-generation hatchery fish and its potential for increased resolution by augmenting the number of polymorphic loci. Given the benefits and disadvantages of the three methods, the combination of mtDNA and microsatellite analyses will best address our research objectives.     

Balancing genetic uniqueness and genetic variation in determining conservation and translocation strategies: a comprehensive case study of threatened dwarf galaxias,Galaxiella pusilla (Mack) (Pisces: Galaxiidae)

Genetic markers are widely used to define and manage populations of threatened species based on the notion that populations with unique lineages of mtDNA and well‐differentiated nuclear marker frequencies should be treated separately. However, a danger of this approach is that genetic uniqueness might be emphasized at the cost of genetic diversity, which is essential for adaptation and is potentially boosted by mixing geographically separate populations. Here, we re‐explore the issue of defining management units, focussing on a detailed study of Galaxiella pusilla, a small freshwater fish of national conservation significance in Australia. Using a combination of microsatellite and mitochondrial markers, 51 populations across the species range were surveyed for genetic structure and diversity. We found an inverse relationship between genetic differentiation and genetic diversity, highlighting a long‐term risk of deliberate isolation of G. pusilla populations based on protection of unique lineages. Instead, we adopt a method for identifying genetic management units that takes into consideration both uniqueness and genetic variation. This produced a management framework to guide future translocation and re‐introduction efforts for G. pusilla, which contrasted to the framework based on a more traditional approach that may overlook important genetic variation in populations.     

Cryptic species within the freshwater isopod Mesamphisopus capensis (Phreatoicidea: Amphisopodidae) in the Western Cape, South Africa: allozyme and 12S rRNA sequence data and morphometric evidence

The freshwater phreatoicidean isopod Mesamphisopus capensis has been regarded as the most widespread of the four Mesamphisopus species occurring in the Western Cape, South Africa. To determine whether this species was monotypic across its distribution over two mountainous regions, separated by a low-lying coastal plain remnant, genetic differentiation among populations from 11 localities was studied through allozyme electrophoresis of 12 loci and sequencing of a 338-bp 12S rRNA mtDNA fragment from representative individuals. Populations of the two regions were separated by a mean identity value of 0.477. Fixed allele differences at two loci distinguished these regions. Estimates of θ indicated substantial differentiation among populations across the entire sample, as well as within each of the regions. Topologies derived through parsimony and neighbour joining supported the monophyly of the two regions. On the basis of these topologies, allele frequencies and an allozyme dendrogram, five groups were identified. Discriminant function analyses, performed on body and pereopod variables independently, revealed these groups to be well differentiated with a high rate of correct a posteriori reclassification. Using genetic distance criteria these five distinct forms may be considered to be putative species. From a conservation perspective, the two regions can be seen to represent two evolutionarily significant units, while the five groups should be regarded as management units.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 235–253.