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.     

Conservation genetics of endangeredBrasenia schreberi based on RAPD and AFLP markers

Brasenia schreberi J.F. Gmelin is a declared endangered species found in the lakes and ponds of South Korea. For planning its conservation strategy, we examined the genetic diversity within and among six populations, using randomly amplified polymorphic DNA (RAPD) and amplified fragment length polymorphism (AFLP). Polymorphisms were more frequently detected per loci with AFLP (69.3%) than RAPD (36.8%). High genetic diversity was recognized within populations: polymorphic loci (PPL) values ranged from 36.3% in the CJM population to 74.5% in the GGT population, with a mean value of 47.8% based on AFLP markers. Great genetic differentiation (θ^B) was detected among the six populations (0.670 on RAPD and 0.196 on AFLP), and we calculated a low rate of gene flow (N_em), i.e., 0.116 on RAPD and 0.977 on AFLP. Furthermore, a Mantel test revealed that no correlation existed between genetic distances and geographical distances among the six local populations, based on RAPD or AFLP markers. These results are attributed to a number of factors, including an insufficient length of time for genetic diversity to be reduced following a natural decline in population size and isolation, adaptation of the genetic system to small population conditions, and a restricted gene flow rate. Based on both its genetic diversity and population structure, we suggest that a strategy for conserving and restoringB. schreberi must focus on maintaining historical processes, such as high levels of outbreeding, while monitoring increased gene flow among populations. This is because a reduction in genetic diversity as a result of genetic drift is undesirable.     

High levels of genetic structuring as a result of population fragmentation in the tropical tree species <Emphasis Type="Italic">Caesalpinia echinata</Emphasis> Lam.

We have investigated levels of genetic diversity within and among seven remnant populations of Caesalpinia echinata Lam., an endangered species found as fragmented populations in three major areas around the coastal regions of Brazil. Using amplified fragment length polymorphism (AFLP) genetic markers, we detected levels of within-population genetic diversity ranging from 0.092 to 0.163, with the lowest values generally being found in the smallest populations. Estimates of between-population genetic differentiation were strongly correlated with geographical distance (r = 0.884, p < 0.001), which,along with a neighbour-joining phylogenetic analysis, strongly suggested high levels of genetic isolation by distance. Over half (62%) of the total genetic diversity was partitioned between populations, further highlighting the genetic distinctness of individual populations. Taken together, these results suggest that fragmentation has led to an increase in population differentiation between fragments of C. echinata. These formations will be of great value in the development of conservation plans for species exhibiting high levels of genetic differentiation due to fragmentation, such as indication of conservation unit size, which populations should be chosen as priority in conservation plans and which samples should be introduced in areas with a low number of individuals of brazilwood.     

Genetic diversity and structure in fragmented populations of the endangered species Ranunculus cabrerensis (Ranunculaceae): implications for conservation

Ranunculus cabrerensis is an endemic and endangered species of the Northwestern Iberian Peninsula. The molecular markers AFLP and ISSR were used to investigate the genetic diversity and population structure of four populations across its known distribution. Fifteen selective primer combinations of AFLP and seventeen ISSR primer combinations produced a total of 2830 and 103 unambiguously repeatable fragments respectively, of which 97.57 and 81.38% were polymorphic for both markers. The genetic diversity of R. cabrerensis at species level was high (H _E = 0.294 by ISSR and H _E = 0.191 by AFLP) and differentiation between sampled locations was also relatively high (G _ST = 0.316 and 0.158 by ISSR and AFLP analysis respectively) compared to other studies of endangered and rare species using the same techniques. The analysis of molecular variance (AMOVA) indicated that the main genetic variation was within sampled locations (73% by AFLP; 52% by ISSR), even though the variation among locations was also significant. Principal Coordinates, NeighborNet and Bayesian analyses revealed a weak but significant relationship between the genetic structures of different populations in R. cabrerensis, with gene flow acting as a homogenizing force that prevents stronger differentiation of populations. Finally, suggestions for conservation strategies to preserve the genetic resources of this species are outlined.     

Cryptic diversity within and amongst spring‐associated Stygobromus amphipods (Amphipoda: Crangonyctidae)

Multiple species of troglomorphic, spring‐associated Stygobromus amphipods, including the endangered, narrow‐range endemic Stygobromus pecki, occupy sites in the Edwards Plateau region of North America. Given the prevalence of cryptic diversity observed in disparate subterranean, animal taxa, we evaluated geographical genetic variation and tested whether Stygobromus contained undetected biodiversity. Nominal Stygobromus taxa were treated as hypotheses and tested with mitochondrial sequence cytochrome oxidase C subunit 1, nuclear sequence (internal transcribed spacer region 1), and AFLP data. Stygobromus pecki population structure and diversity was characterized and compared with congeners. For several Stygobromus species, the nominal taxonomy conflicted with molecular genetic data and there was strong evidence of significant cryptic diversity. Whereas S. pecki genetic diversity was similar to that of congeners, mitochondrial data identified two significantly diverged but sympatric clades. AFLP data for S. pecki indicated relatively recent and ongoing gene flow in the nuclear genome. These data for S. pecki suggest either a substantial history of isolation followed by current sympatry and ongoing admixture, or a protracted period of extremely large effective population size. This study demonstrates that Edwards Plateau Stygobromus are a complex, genetically diverse group with substantially more diversity than currently recognized. © 2013 The Linnean Society of London     

Genetic diversity of the endangered Chinese endemic herb Primulina tabacum (Gesneriaceae) revealed by amplified fragment length polymorphism (AFLP)

Primulina tabacum Hance, is a critically endangered perennial endemic to limestone area in South China. Genetic variability within and among four extant populations of this species was assessed using AFLP markers. We expected a low genetic diversity level of this narrowly distributed species, but our results revealed that a high level of genetic diversity remains, both at population level (55.5% of markers polymorphic, H _E = 0.220, I _S = 0.321), and at species level (P = 85.6% of markers polymorphic, H _E = 0.339, I _S = 0.495), probably resulting from its refugial history and/or breeding system. High levels of genetic differentiation among populations was apparent based on Nei’s genetic diversity analysis (G _st=0.350). The restricted gene flow between populations is a potential reason for the high genetic differentiation. The population genetic diversity of P. tabacum revealed here has clear implications for conservation and management. To maintain present levels of genetic diversity, in situ conservation of all populations is necessary.     

AFLP and ISSR analysis reveals high genetic variation and inter-population differentiation in fragmented populations of the endangered Litsea szemaois (Lauraceae) from Southwest China

Litsea szemaois (Lauraceae) is an endemic and endangered species from the tropical rain forests of Xishuangbanna, southern Yunnan, SW China, but habitat fragmentation, especially exacerbated by rubber planting, has caused a decline in population size of the species. AFLP and ISSR were used to investigate the genetic diversity and population structure of eight populations from across its known distribution. Three AFLP and ten ISSR primer combinations produced a total of 203 and 77 unambiguous and repeatable bands respectively, of which 164 (80.8%) and 67 (87.0%) were polymorphic for the two markers. These two markers showed that Litsea szemaois exhibits comparatively high genetic diversity at species level (heterozygosity (hs) = 0.2109) relative to some other Lauraceae. Most of the genetic variation was partitioned within populations, but genetic differentiation between populations was significant and relatively high (Φ _st = 0.2420, θ^B = 0.1986) compared with other tropical plants. The genetic characteristics of L. szemaois may be related to its outbreeding system, insect pollination and fragmented distribution. Because L. szemaois is dioecious and slow to mature, ex situ conservation across its genetic diversity is unlikely to succeed, although seedlings grow well under cultivation. Thus, in situ conservation is very important for this endangered species, especially as only 133 adult individuals are known in the wild. In particular, the Nabanhe and Mandian populations should be given a high conservation priority due to their higher genetic diversity, larger population size and better field condition, but wider sampling is required across all populations to determine additional areas with significant genetic conservation value.     

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.     

Isolation and characterization of 15 microsatellite loci in the Korean goral (Nemorhaedus caudatus)

Microsatellites have been applied in a variety of fields, including conservation genetics. Species‐specific microsatellites are considered as more powerful genetic markers to generate an accurate genetic composition of a species itself. Accordingly, we characterized 15 polymorphic microsatellite loci from Korean goral, Nemorhaedus caudatus, one of the most endangered species in South Korea. The new markers should benefit future studies of the endangered species of other Asian gorals and their relatives for the study of genetic diversity and potential conservation management.     

Higher β‐ and γ‐diversity at species and genetic levels in headwaters than in mid‐order streams in Hydropsyche (Trichoptera)

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The genetic diversity and spatial genetic structure of the Corso‐Sardinian endemic Ferula arrigonii Bocchieri (Apiaceae)

Corsica and Sardinia represent major hotspots of plant diversity in the Mediterranean area and are priority regions for conservation due to their high number of endemic plant species. However, information supporting human decision‐making on the conservation of these species is still scarce, especially at the genetic level. In this work, the first assessment is reported of the species‐wide spatial genetic structure and diversity of Ferula arrigonii Bocchieri, a Corso‐Sardinian endemic located in a few coastal sites and on small islands. Nine populations covering the entire natural range of the species were investigated by means of AFLP (amplified fragment length polymorphism) markers. Results indicate that this species is characterised by high levels of genetic polymorphism (92% polymorphic fragments) and of genetic diversity (H_w = 0.317) and by relatively low differentiation among populations (F_st = 0.057). PCoA, Bayesian analysis and neighbour‐joining clustering were also employed to investigate the genetic structure of this species. Three genetically distinct groups were detected, although with considerable overlap between populations.     

GENETIC STRUCTURE IN POPULATIONS OF FUCUS VESICULOSUS (PHAEOPHYCEAE) OVER SPATIAL SCALES FROM 10 M TO 800 KM1

Recent studies showing consequences of species’ genetic diversity on ecosystem performance raise the concern of how key ecosystem species are genetically structured. The bladder wrack Fucus vesiculosus L. is a dominant species of macroalga in the northern Atlantic, and it is particularly important as a habitat‐forming species in the Baltic Sea. We examined the genetic structure of populations of F. vesiculosus with a hierarchical approach from a within‐shore scale (10 m) to a between‐seas scale (Baltic Sea–Skagerrak, 800 km). Analysis of five microsatellite loci showed that population differentiation was generally strong (average F_ST = 12%), being significant at all spatial scales investigated (10¹, 10³, 10^4–5, 10⁶ m). Genetic differentiation between seas (Baltic Sea and Skagerrak) was substantial. Nevertheless, the effects of isolation by distance were stronger within seas than between seas. Notably, Baltic summer‐reproducing populations showed a strong within‐sea, between‐area (70 km) genetic structure, while Baltic autumn‐reproducing populations and Skagerrak summer‐reproducing populations revealed most genetic diversity between samples within areas (<1 km). Despite such differences in overall structure, Baltic populations of summer‐ and autumn‐reproducing morphs did not separate in a cluster analysis, indicating minor, if any, barriers to gene flow between them. Our results have important implications for management and conservation of F. vesiculosus, and we raise a number of concerns about how genetic variability should be preserved within this species.     

Restricted dispersal and genetic diversity in populations of an endangered montane lizard (Eulamprus leuraensis,Scincidae)

Many alpine species are under threat from global climate change, as their geographic ranges become increasingly fragmented and unsuitable. Understanding rates and determinants of gene flow among such fragmented populations, over historical as well as recent timescales, can help to identify populations under threat. It is also important to clarify the degree to which loss of local populations reduces overall genetic diversity within the taxon. The endangered Blue Mountains Water Skink (Eulamprus leuraensis) is restricted to <40 small swamps in montane south‐eastern Australia. Our analyses of seven microsatellite loci of 241 animals from 13 populations show strong geographic structure, with major genetic divergence even between populations separated by <0.5 km. Dispersal between populations is scarce, and appears to involve mostly males. Our analyses suggest potential recent bottleneck events in all the identified populations, and lower genetic diversity and population size parameter at lower‐elevation sites than at higher‐elevation sites. Management of this endangered taxon thus needs to treat most populations separately, because of their genetic distinctiveness and low rates of genetic exchange.     

Low genetic diversity and fragmentation effects in a wind-pollinated tree, Polylepis multijuga Plige (Rosaceae) in the high Andes

Fragmentation is predicted to increase inbreeding depression and lower the evolutionary potential of organisms by disrupting dispersal. Trees may be more resilient to fragmentation effects due to potential long-distance dispersal mechanisms that genetically connect fragments. Polylepis woodlands in the high Andes are highly fragmented and are currently the focus of reforestation and conservation efforts. Polylepis multijuga Plige (Rosaceae) is a threatened, endemic tree species in the northern Andes of Peru. Samples were collected from 371 adult trees in nine forest fragments separated by 0.5–80 km and genotyped at amplified fragment length polymorphism loci (AFLP) and chloroplast intergenic regions to determine the connectedness of fragments and their suitability for collecting seed for restoration efforts. P. multijuga is wind-pollinated and dispersed; however, genetic diversity in P. multijuga was about half that reported for other wind-pollinated species. Genetic spatial autocorrelation and patterns of chloroplast and AFLP diversity suggest seed dispersal is very limited and that wind dispersed pollen does not effectively connect all fragments. Conservation of this species will require reforestation efforts and possibly augmentation of some fragments to increase their genetic diversity. Collecting seed from multiple large fragments and from individuals separated by at least 25 m within fragments would maximize the genetic diversity of seed collections for reforestation or augmentation. Future studies of this and other Polylepis species should determine how complex topography may affect wind mediated dispersal between fragments and patterns of genetic diversity.     

Narrow endemics to Mediterranean islands: Moderate genetic diversity but narrow climatic niche of the ancient,critically endangered Naufraga (Apiaceae)

Narrow endemics constitute the cornerstone of Mediterranean plant diversity. Naufraga balearica (Apiaceae) is a critically endangered, extremely narrow endemic plant from the western Mediterranean island of Majorca. Because the species belongs to a monotypic genus, N. balearica was hypothesized to be a palaeoendemism. Here we conducted phylogenetic dating, population genetic and climatic niche analyses in order to understand the evolutionary history and conservation perspectives of this flagship species. Phylogenetic dating analysis of nuclear and plastid DNA sequences revealed a late Miocene to early Pliocene divergence between Naufraga and its sister genus Apium, supporting the palaeoendemic status of the former. Amplified fragment length polymorphism (AFLP) markers and plastid DNA sequences of the five Naufraga populations revealed moderate genetic diversity. This diversity is in line with that of other palaeoendemisms from western Mediterranean islands, as revealed by a comparison with 22 other narrow endemic species from this region. Despite the fact that all Naufraga populations are located at a maximum distance of 10 km in a straight line, a strikingly strong population differentiation was found for AFLP markers, which is explained by long-term isolation likely related to short-range pollination and dispersal strategies of the species. While the species is not genetically impoverished, species distribution modelling and microclimatic monitoring revealed that narrow ecological requirements underlie the current extreme rarity of Naufraga and may jeopardize its long-term survival. Our results indicate that a multidisciplinary approach provides powerful tools to develop conservation strategies for evolutionarily singular lineages.     

The influence of spatial scale on the genetic structure of a widespread tropical wetland tree, Pterocarpus officinalis (Fabaceae)

Identifying factors that cause genetic differentiation in plant populations and the spatial scale at which genetic structuring can be detected will help to understand plant population dynamics and identify conservation units. In this study, we determined the genetic structure and diversity of Pterocarpus officinalis, a widespread tropical wetland tree, at three spatial scales: (1) drainage basin “watershed” (<10 km), (2) within Puerto Rico (<100 km), and (3) Caribbean-wide (>1000 km) using AFLP. At all three spatial scales, most of the genetic variation occurred within populations, but as the spatial scale increased from the watershed to the Caribbean region, there was an increase in the among population variation (Φ_ST=0.19 to Φ_ST=0.53). At the watershed scale, there was no significant differentiation (P=0.77) among populations in the different watersheds, although there was some evidence that montane and coastal populations differed (P<0.01). At the island scale, there was significant differentiation (P<0.001) among four populations in Puerto Rico. At the regional scale (>1000 km), we found significant differentiation (P<0.001) between island and continental populations in the Caribbean region, which we attributed to factors associated with the colonization history of P. officinalis in the Neotropics. Given that genetic structure can occur from local to regional spatial scales, it is critical that conservation recommendations be based on genetic information collected at the appropriate spatial scale.     

Genetic diversity of small populations: Not always “doom and gloom”?

Is a key theory of evolutionary and conservation biology—that loss of genetic diversity can be predicted from population size—on shaky ground? In the face of increasing human‐induced species depletion and habitat fragmentation, this question and the study of genetic diversity in small populations are paramount to understanding the limits of species’ responses to environmental change and to providing remedies to endangered species conservation. Few empirical studies have investigated to what degree some small populations might be buffered against losses of genetic diversity. Even fewer studies have experimentally tested the potential underlying mechanisms. The study of Schou, Loeschcke, Bechsgaard, Schlotterer, and Kristensen ( 2017 ) in this issue of Molecular Ecology is elegant in combining classic common garden experimentation with population genomics on an iconic experimental model species (Drosophila melanogaster). The authors reveal a slower rate of loss of genetic diversity in small populations under varying thermal regimes than theoretically expected and hence an unexpected retention of genetic diversity. They are further able to hone in on a plausible mechanism: associative overdominance, wherein homozygosity of deleterious recessive alleles is especially disfavoured in genomic regions of low recombination. These results contribute to a budding literature on the varying mechanisms underlying genetic diversity in small populations and encourage further such research towards the effective management and conservation of fragmented or endangered populations.     

Genetic analysis and conservation of the endangered Canary Island woody sow-thistle, Sonchus gandogeri (Asteraceae)

Sonchus gandogeri, a woody sow-thistle, is an endangered Canary Island endemic with only two known populations, one in the El Golfo and another in the Las Esperillas of El Hierro. Amplified fragment length polymorphism (AFLP) markers were used to assess the genetic variation within and among populations. The mean genetic diversity of two populations was estimated to be 0.380, and the El Golfo population (0.380) had higher genetic diversity than the southeastern one (0.268). The unbiased Neis genetic identity between the two populations was 0.846. The mean genetic diversity of S. gandogeri was much higher than that of the other endangered plant species. This is perhaps due to breeding system, life form, extinction, and/or introgressive hybridization and hybrid origin of the taxon. This study also indicates that the two populations are not strongly differentiated (G_ST=0.149). This study suggests that S. gandogeri is more likely to become extinct due to environmental or demographic forces than genetic factors, such as inbreeding depression. More strict control of introduced herbivores is necessary to protect these populations, and germplasm collection for ex situ conservation is needed.     

‘Good-genes’ and ‘compatible-genes’ effects in an Alpine whitefish and the information content of breeding tubercles over the course of the spawning season

Abies ziyuanensis is a highly endangered fir species endemic to South China. Unlike other Abies species that are distributed in areas with cold climates, A. ziyuanensis is restricted to several isolated island-like localities at subtropical mountains. In this study, we used dominant amplified fragment length polymorphism (AFLP) and co-dominant simple sequence repeats (SSR) markers to infer the genetic structure of A. ziyuanensis. Seven populations consisting of 139 individuals were sampled across their whole distribution. A. ziyuanenesis has a relatively low level of genetic variation, with a mean genetic diversity per population (He) of 0.136 (AFLP) and 0.337 (SSR), which is lower than that of other reported endemic species based on the same kind of marker. We observed high population differentiation, with Gst = 0.482 (AFLP) and Fst = 0.250 (SSR), among the seven populations. AMOVA also detected significant differentiation among populations (Φst (AFLP) = 0.550 and Φst (SSR) = 0.289) and among regions (Φct (AFLP) = 0.139 and Φct (SSR) = 0.135) in both marker types. Both ongoing evolutionary forces (e.g., genetic drift resulting from small population size) and historical events (e.g., population contraction and fragmentation during and after the Quaternary glacial cycles) may have contributed to the genetic structure in A. ziyuanensis.