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1.  The Complete Maternally and Paternally Inherited Mitochondrial Genomes of the Endangered Freshwater Mussel Solenaia carinatus (Bivalvia: Unionidae) and Implications for Unionidae Taxonomy 
PLoS ONE  2013;8(12):e84352.
Doubly uniparental inheritance (DUI) is an exception to the typical maternal inheritance of mitochondrial (mt) DNA in Metazoa, and found only in some bivalves. In species with DUI, there are two highly divergent gender-associated mt genomes: maternal (F) and paternal (M), which transmit independently and show different tissue localization. Solenaia carinatus is an endangered freshwater mussel species exclusive to Poyang Lake basin, China. Anthropogenic events in the watershed greatly threaten the survival of this species. Nevertheless, the taxonomy of S. carinatus based on shell morphology is confusing, and the subfamilial placement of the genus Solenaia remains unclear. In order to clarify the taxonomic status and discuss the phylogenetic implications of family Unionidae, the entire F and M mt genomes of S. carinatus were sequenced and compared with the mt genomes of diverse freshwater mussel species. The complete F and M mt genomes of S. carinatus are 16716 bp and 17102 bp in size, respectively. The F and M mt genomes of S. carinatus diverge by about 40% in nucleotide sequence and 48% in amino acid sequence. Compared to F counterparts, the M genome shows a more compact structure. Different gene arrangements are found in these two gender-associated mt genomes. Among these, the F genome cox2-rrnS gene order is considered to be a genome-level synapomorphy for female lineage of the subfamily Gonideinae. From maternal and paternal mtDNA perspectives, the phylogenetic analyses of Unionoida indicate that S. carinatus belongs to Gonideinae. The F and M clades in freshwater mussels are reciprocal monophyly. The phylogenetic trees advocate the classification of sampled Unionidae species into four subfamilies: Gonideinae, Ambleminae, Anodontinae, and Unioninae, which is supported by the morphological characteristics of glochidia.
PMCID: PMC3866145  PMID: 24358356
2.  Incongruence between mtDNA and nuclear data in the freshwater mussel genus Cyprogenia (Bivalvia: Unionidae) and its impact on species delineation 
Ecology and Evolution  2016;10.1002/ece3.2071.
Accurately identifying species is a crucial step for developing conservation strategies for freshwater mussels, one of the most imperiled faunas in North America. This study uses genetic data to re‐examine species delineation in the genus Cyprogenia. Historically, Cyprogenia found west of the Mississippi River have been ascribed to Cyprogenia aberti (Conrad 1850), and those east of the Mississippi River were classified as Cyprogenia stegaria (Rafinesque 1820). Previous studies using mitochondrial DNA sequences indicated that C. aberti and C. stegaria were not reciprocally monophyletic groups, suggesting the need for systematic revision. We generated a novel dataset consisting of 10 microsatellite loci and combined it with sequence data from the mitochondrial ND1 gene for 223 Cyprogenia specimens. Bayesian analysis of the ND1 nucleotide sequences identified two divergent clades that differ by 15.9%. Members of these two clades occur sympatrically across most sampling locations. In contrast, microsatellite genotypes support recognition of three allopatric clusters defined by major hydrologic basins. The divergent mitochondrial lineages are highly correlated with the color of the conglutinate lures used by mussels to attract and infest host fishes, and tests for selection at the ND1 locus were positive. We infer that the incongruence between mtDNA and microsatellite data in Cyprogenia may be the result of a combination of incomplete lineage sorting and balancing selection on lure color. Our results provide further evidence that mitochondrial markers are not always neutral with respect to selection, and highlight the potential problems of relying on a single‐locus‐marker for delineating species.
PMCID: PMC4788976  PMID: 27066233
Conservation; mito‐nuclear discordance; population genetics; unionid
3.  Incongruence between mtDNA and nuclear data in the freshwater mussel genus Cyprogenia (Bivalvia: Unionidae) and its impact on species delineation 
Ecology and Evolution  2016;6(8):2439-2452.
Accurately identifying species is a crucial step for developing conservation strategies for freshwater mussels, one of the most imperiled faunas in North America. This study uses genetic data to re‐examine species delineation in the genus Cyprogenia. Historically, Cyprogenia found west of the Mississippi River have been ascribed to Cyprogenia aberti (Conrad 1850), and those east of the Mississippi River were classified as Cyprogenia stegaria (Rafinesque 1820). Previous studies using mitochondrial DNA sequences indicated that C. aberti and C. stegaria were not reciprocally monophyletic groups, suggesting the need for systematic revision. We generated a novel dataset consisting of 10 microsatellite loci and combined it with sequence data from the mitochondrial ND1 gene for 223 Cyprogenia specimens. Bayesian analysis of the ND1 nucleotide sequences identified two divergent clades that differ by 15.9%. Members of these two clades occur sympatrically across most sampling locations. In contrast, microsatellite genotypes support recognition of three allopatric clusters defined by major hydrologic basins. The divergent mitochondrial lineages are highly correlated with the color of the conglutinate lures used by mussels to attract and infest host fishes, and tests for selection at the ND1 locus were positive. We infer that the incongruence between mtDNA and microsatellite data in Cyprogenia may be the result of a combination of incomplete lineage sorting and balancing selection on lure color. Our results provide further evidence that mitochondrial markers are not always neutral with respect to selection, and highlight the potential problems of relying on a single‐locus‐marker for delineating species.
PMCID: PMC4788976  PMID: 27066233
Conservation; mito‐nuclear discordance; population genetics; unionid
4.  Species distribution modelling for conservation of an endangered endemic orchid 
AoB Plants  2015;7:plv039.
Navasota ladies'-tresses is an orchid native to eastern and central Texas. It was listed as endangered by the U.S. Fish and Wildlife Service in 1982 and by the State of Texas soon afterwards. Wang et al. (2015) analyzed field data collected over nine years to identify areas of critical habitat, areas into which the species could expand its range, and areas that might serve as conservation corridors. These results will provide valuable information for those interested in conservation and management of this endangered orchid as well as a framework for the development of future studies of this and other endangered plants.
Concerns regarding the long-term viability of threatened and endangered plant species are increasingly warranted given the potential impacts of climate change and habitat fragmentation on unstable and isolated populations. Orchidaceae is the largest and most diverse family of flowering plants, but it is currently facing unprecedented risks of extinction. Despite substantial conservation emphasis on rare orchids, populations continue to decline. Spiranthes parksii (Navasota ladies' tresses) is a federally and state-listed endangered terrestrial orchid endemic to central Texas. Hence, we aimed to identify potential factors influencing the distribution of the species, quantify the relative importance of each factor and determine suitable habitat for future surveys and targeted conservation efforts. We analysed several geo-referenced variables describing climatic conditions and landscape features to identify potential factors influencing the likelihood of occurrence of S. parksii using boosted regression trees. Our model classified 97 % of the cells correctly with regard to species presence and absence, and indicated that probability of existence was correlated with climatic conditions and landscape features. The most influential variables were mean annual precipitation, mean elevation, mean annual minimum temperature and mean annual maximum temperature. The most likely suitable range for S. parksii was the eastern portions of Leon and Madison Counties, the southern portion of Brazos County, a portion of northern Grimes County and along the borders between Burleson and Washington Counties. Our model can assist in the development of an integrated conservation strategy through: (i) focussing future survey and research efforts on areas with a high likelihood of occurrence, (ii) aiding in selection of areas for conservation and restoration and (iii) framing future research questions including those necessary for predicting responses to climate change. Our model could also incorporate new information on S. parksii as it becomes available to improve prediction accuracy, and our methodology could be adapted to develop distribution maps for other rare species of conservation concern.
PMCID: PMC4463238  PMID: 25900746
Boosted regression trees; conservation; endangered species; Navasota ladies’ tresses; reintroduction; species distribution models
5.  The Complete Maternally and Paternally Inherited Mitochondrial Genomes of a Freshwater Mussel Potamilus alatus (Bivalvia: Unionidae) 
PLoS ONE  2017;12(1):e0169749.
Doubly uniparental inheritance (DUI) of mitochondrial DNA, found only in some bivalve families and characterized by the existence of gender-associated mtDNA lineages that are inherited through males (M-type) or females (F-type), is one of the very few exceptions to the general rule of strict maternal mtDNA inheritance in animals. M-type sequences are often undetected and hence still underrepresented in the GenBank, which hinders the progress of the understanding of the DUI phenomenon. We have sequenced and analyzed the complete M and F mitogenomes of a freshwater mussel, Potamilus alatus. The M-type was 493 bp longer (M = 16 560, F = 16 067 bp). Gene contents, order and the distribution of genes between L and H strands were typical for unionid mussels. Candidates for the two ORFan genes (forf and morf) were found in respective mitogenomes. Both mitogenomes had a very similar A+T bias: F = 61% and M = 62.2%. The M mitogenome-specific cox2 extension (144 bp) is much shorter than in other sequenced unionid mitogenomes (531–576 bp), which might be characteristic for the Potamilus genus. The overall topology of the phylogenetic tree is in very good agreement with the currently accepted phylogenetic relationships within the Unionidae: both studied sequences were placed within the Ambleminae subfamily clusters in the corresponding M and F clades.
PMCID: PMC5222514  PMID: 28068380
6.  Phylogenetic and morphometric analyses reveal ecophenotypic plasticity in freshwater mussels Obovaria jacksoniana and Villosa arkansasensis (Bivalvia: Unionidae) 
Ecology and Evolution  2013;3(8):2670-2683.
Freshwater mollusk shell morphology exhibits clinal variation along a stream continuum that has been termed the Law of Stream Distribution. We analyzed phylogenetic relationships and morphological similarity of two freshwater mussels (Bivalvia: Unionidae), Obovaria jacksoniana and Villosa arkansasensis, throughout their ranges. The objectives were to investigate phylogenetic structure and evolutionary divergence of O. jacksoniana and V. arkansasensis and morphological similarity between the two species. Our analyses were the first explicit tests of phenotypic plasticity in shell morphologies using a combination of genetics and morphometrics. We conducted phylogenetic analyses of mitochondrial DNA (1416 bp; two genes) and morphometric analyses for 135 individuals of O. jacksoniana and V. arkansasensis from 12 streams. We examined correlations among genetic, morphological, and spatial distances using Mantel tests. Molecular phylogenetic analyses revealed a monophyletic relationship between O. jacksoniana and V. arkansasensis. Within this O. jacksoniana/V. arkansasensis complex, five distinct clades corresponding to drainage patterns showed high genetic divergence. Morphometric analysis revealed relative differences in shell morphologies between the two currently recognized species. We conclude that morphological differences between the two species are caused by ecophenotypic plasticity. A series of Mantel tests showed regional and local genetic isolation by distance. We observed clear positive correlations between morphological and geographic distances within a single drainage. We did not observe correlations between genetic and morphological distances. Phylogenetic analyses suggest O. jacksoniana and V. arkansasensis are synonomous and most closely related to a clade composed of O. retusa, O. subrotunda, and O. unicolor. Therefore, the synonomous O. jacksoniana and V. arkansasensis should be recognized as Obovaria arkansasensis (Lea 1862) n. comb. Phylogenetic analyses also showed relative genetic isolation among drainages, suggesting no current gene flow. Further investigation of in-progress speciation and/or cryptic species within O. arkansasensis is warranted followed by appropriate revision of conservation management designations.
In this study, we found Obovaria jacksoniana and Villosa arkansasensis are synonomous. We suggest that morphological differences between the two species are caused by ecophenotypic plasticity, where V. arkansasensis is the upstream morphotype and O. jacksoniana is the downstream morphotype of a single species.
PMCID: PMC3930048  PMID: 24567831
Isolation by distance; Law of Stream Distribution; Mantel test; mitochondrial DNA; Ortmann's law; phenotypic plasticity
7.  Complex population genetic and demographic history of the Salangid, Neosalanx taihuensis, based on cytochrome b sequences 
The Salangid icefish Neosalanx taihuensis (Salangidae) is an economically important fish, which is endemic to China, restricted to large freshwater systems (e.g. lakes, large rivers and estuaries) and typically exhibit low vagility. The continuous distribution ranges from the temperate region of the Huai and Yellow River basins to the subtropical region of the Pearl River basin. This wide ranging distribution makes the species an ideal model for the study of palaeoclimatic effects on population genetic structure and phylogeography. Here, we aim to analyze population genetic differentiation within and between river basins and demographic history in order to understand how this species responded to severe climatic oscillations, decline of the sea levels during the Pleistocene ice ages and tectonic activity.
We obtained the complete mtDNA cytochrome b sequences (1141 bp) of 354 individuals from 13 populations in the Pearl River, the Yangze River and the Huai River basin. Thirty-six haplotypes were detected. Haplotype frequency distributions were strongly skewed, with most haplotypes (n = 24) represented only in single samples each and thus restricted to a single population. The most common haplotype (H36) was found in 49.15% of all individuals. Analysis of molecular variance (AMOVA) revealed a random pattern in the distribution of genetic diversity, which is inconsistent with contemporary hydrological structure. Significant levels of genetic subdivision were detected among populations within basins rather than between the three basins. Demographic analysis revealed that the population size in the Pearl River basin has remained relatively constant whereas the populations in the Yangze River and the Huai River basins expanded about 221 and 190 kyr ago, respectively, with the majority of mutations occurring after the last glacial maximum (LGM).
The observed complex genetic pattern of N. taihuensis is coherent with a scenario of multiple unrelated founding events by long-distance colonization and dispersal combined with contiguous population expansion and locally restricted gene flow. We also found that this species was likely severely impacted by past glaciations. More favourable climate and the formation of large suitable habitations together facilitated population expansion after the late Quaternary (especially the LGM). We proposed that all populations should be managed and conserved separately, especially for habitat protection.
PMCID: PMC2483725  PMID: 18625046
8.  Cytotaxonomy of unionid freshwater mussels (Unionoida, Unionidae) from northeastern Thailand with description of a new species 
ZooKeys  2015;93-110.
Morphological and chromosomal characteristics of a number of unionid freshwater mussels were studied from northeastern Thailand. Karyotypes of eight species from seven genera (Chamberlainia, Ensidens, Hyriopsis, Physunio, Pseudodon, Scabies and Trapezoideus) were examined. Six species possess 2n = 38 karyotypes, whereas Scabies crispata and an unidentified Scabies sp. lack three small chromosome pairs, giving a diploid number of 32. Moreover, the karyotypes of the unidentified Scabies differ from Scabies crispata as it exhibits a telocentric chromosome pair (6m + 7sm + 2st + 1t). Most of the conchological characters also differ between the two species – adult size, colour pattern, muscle scars, pseudocardinal and lateral teeth. The name Scabies songkramensis sp. n. is proposed for the unidentified species, and its description is included in this paper. Interestingly, seven species contain mostly bi-armed chromosomes, but only the mud-dweller in stagnant water, Ensidens ingallsianus, contains predominantly five telocentric pairs. In addition, the marker chromosome characteristics of an unbalanced long arm, twisted centromere, a wider angle 180° arrangement, a twisted arm and telomeric end union reported in this study are described for the first time for unionid mussels.
PMCID: PMC4525026  PMID: 26261434
Chromosome; mussel; karyotype; systematics; Southeast Asia; cryptic species
9.  Chagas Disease Risk in Texas 
Chagas disease, caused by Trypanosoma cruzi, remains a serious public health concern in many areas of Latin America, including México. It is also endemic in Texas with an autochthonous canine cycle, abundant vectors (Triatoma species) in many counties, and established domestic and peridomestic cycles which make competent reservoirs available throughout the state. Yet, Chagas disease is not reportable in Texas, blood donor screening is not mandatory, and the serological profiles of human and canine populations remain unknown. The purpose of this analysis was to provide a formal risk assessment, including risk maps, which recommends the removal of these lacunae.
Methods and Findings
The spatial relative risk of the establishment of autochthonous Chagas disease cycles in Texas was assessed using a five–stage analysis. 1. Ecological risk for Chagas disease was established at a fine spatial resolution using a maximum entropy algorithm that takes as input occurrence points of vectors and environmental layers. The analysis was restricted to triatomine vector species for which new data were generated through field collection and through collation of post–1960 museum records in both México and the United States with sufficiently low georeferenced error to be admissible given the spatial resolution of the analysis (1 arc–minute). The new data extended the distribution of vector species to 10 new Texas counties. The models predicted that Triatoma gerstaeckeri has a large region of contiguous suitable habitat in the southern United States and México, T. lecticularia has a diffuse suitable habitat distribution along both coasts of the same region, and T. sanguisuga has a disjoint suitable habitat distribution along the coasts of the United States. The ecological risk is highest in south Texas. 2. Incidence–based relative risk was computed at the county level using the Bayesian Besag–York–Mollié model and post–1960 T. cruzi incidence data. This risk is concentrated in south Texas. 3. The ecological and incidence–based risks were analyzed together in a multi–criteria dominance analysis of all counties and those counties in which there were as yet no reports of parasite incidence. Both analyses picked out counties in south Texas as those at highest risk. 4. As an alternative to the multi–criteria analysis, the ecological and incidence–based risks were compounded in a multiplicative composite risk model. Counties in south Texas emerged as those with the highest risk. 5. Risk as the relative expected exposure rate was computed using a multiplicative model for the composite risk and a scaled population county map for Texas. Counties with highest risk were those in south Texas and a few counties with high human populations in north, east, and central Texas showing that, though Chagas disease risk is concentrated in south Texas, it is not restricted to it.
For all of Texas, Chagas disease should be designated as reportable, as it is in Arizona and Massachusetts. At least for south Texas, lower than N, blood donor screening should be mandatory, and the serological profiles of human and canine populations should be established. It is also recommended that a joint initiative be undertaken by the United States and México to combat Chagas disease in the trans–border region. The methodology developed for this analysis can be easily exported to other geographical and disease contexts in which risk assessment is of potential value.
Author Summary
Chagas disease is endemic in Texas and spread through triatomine insect vectors known as kissing bugs, assassin bugs, or cone–nosed bugs, which transmit the protozoan parasite, Trypanosoma cruzi. We examined the threat of Chagas disease due to the three most prevalent vector species and from human case occurrences and human population data at the county level. We modeled the distribution of each vector species using occurrence data from México and the United States and environmental variables. We then computed the ecological risk from the distribution models and combined it with disease incidence data to produce a composite risk map which was subsequently used to calculate the populations expected to be at risk for the disease. South Texas had the highest relative risk. We recommend mandatory reporting of Chagas disease in Texas, testing of blood donations in high risk counties, human and canine testing for Chagas disease antibodies in high risk counties, and that a joint initiative be developed between the United States and México to combat Chagas disease.
PMCID: PMC2950149  PMID: 20957148
10.  Sinanodonta Woodiana (Mollusca: Bivalvia: Unionidae): Isolation and Characterization of the First Microsatellite Markers 
Sinanodonta woodiana (Lea, 1834) is a large Unionid species with a real invasion success. It colonized Europe, Central America, the Indonesian Islands and recently North America. The species life cycle involves a larval parasitic stage on freshwater fish species which contributes to the spread of the mussel. In this paper we describe, for the first time, eight polymorphic microsatellite loci for the species Sinanodonta woodiana. The genetic screening of individuals confirmed that all loci were highly polymorphic. The number of alleles per locus ranged from 7 to 14 and the observed heterozygosity ranged from 0.650 to 0.950. These loci should prove useful to study the species population genetics which could help to infer important aspects of the invasion process.
PMCID: PMC3179163  PMID: 21954356
invasive species; microsatellite; population genetics; range expansion; native area
11.  Bioaccumulation of selected metals in bivalves (Unionidae) and Phragmites australis inhabiting a municipal water reservoir 
Urbanization can considerably affect water reservoirs by, inter alia, input, and accumulation of contaminants including metals. Located in the course of River Cybina, Maltański Reservoir (Western Poland) is an artificial shallow water body built for recreation and sport purposes which undergoes restoration treatment (drainage) every 4 years. In the present study, we demonstrate an accumulation of nine metals (Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Zn) in water, sediment, three bivalve species (Anodonta anatina, Anodonta cygnea, Unio tumidus), and macrophyte Phragmites australis collected before complete drainage in November 2012. The mean concentrations of metals in the sediment, bivalves, and P. australis (roots and leaves) decreased in the following order: Fe > Mn > Zn > Cu > Cr > Ni > Pb > Co > Cd. A considerably higher bioconcentration of metals was observed in samples collected from the western and southern sites which undergo a higher degree of human impact. Sediments were found to be a better indicator of metal contamination than water samples. Interspecific differences in levels of metal accumulation were found between investigated unionids. U. tumidus accumulated higher levels of Cr, positively correlated with ambient concentrations, predisposing this species as a potential bioindicator of this metal in aquatic environments. On the other hand, species of Anodonta genus demonstrated higher accumulation of Cu and Cd. Positive correlations were found between Pb content in the sediments and tissues of all three bivalve species. In P. australis, metals were largely retained in roots except for Cd and Pb for which higher concentrations were found in leaves suggesting additional absorption of these metals from aerial sources. P. australis and bivalve from the Maltański Reservoir may be a potential source of toxic metals for animals feeding upon them and contribute to further contamination in the food chain.
Electronic supplementary material
The online version of this article (doi:10.1007/s10661-013-3610-8) contains supplementary material, which is available to authorized users.
PMCID: PMC3969812  PMID: 24407963
Heavy metals; Bivalve; Common reed; Bioaccumulation; Water reservoir
12.  Complex evolutionary history of the Mexican stoneroller Campostoma ornatum Girard, 1856 (Actinopterygii: Cyprinidae) 
Studies of the phylogeography of Mexican species are steadily revealing genetic patterns shared by different species, which will help to unravel the complex biogeographic history of the region. Campostoma ornatum is a freshwater fish endemic to montane and semiarid regions in northwest Mexico and southern Arizona. Its wide range of distribution and the previously observed morphological differentiation between populations in different watersheds make this species a useful model to investigate the biogeographic role of the Sierra Madre Occidental and to disentangle the actions of Pliocene tecto-volcanic processes vs Quaternary climatic change. Our phylogeographic study was based on DNA sequences from one mitochondrial gene (cytb, 1110 bp, n = 285) and two nuclear gene regions (S7 and RAG1, 1822 bp in total, n = 56 and 43, respectively) obtained from 18 to 29 localities, in addition to a morphological survey covering the entire distribution area. Such a dataset allowed us to assess whether any of the populations/lineages sampled deserve to be categorised as an evolutionarily significant unit.
We found two morphologically and genetically well-differentiated groups within C. ornatum. One is located in the northern river drainages (Yaqui, Mayo, Fuerte, Sonora, Casas Grandes, Santa Clara and Conchos) and another one is found in the southern drainages (Nazas, Aguanaval and Piaxtla). The split between these two lineages took place about 3.9 Mya (CI = 2.1-5.9). Within the northern lineage, there was strong and significant inter-basin genetic differentiation and also several secondary dispersal episodes whit gene homogenization between drainages. Interestingly, three divergent mitochondrial lineages were found in sympatry in two northern localities from the Yaqui river basin.
Our results indicate that there was isolation between the northern and southern phylogroups since the Pliocene, which was related to the formation of the ancient Nazas River paleosystem, where the southern group originated. Within groups, a complex reticulate biogeographic history for C. ornatum populations emerges, following the taxon pulse theory and mainly related with Pliocene tecto-volcanic processes. In the northern group, several events of vicariance promoted by river or drainage isolation episodes were found, but within both groups, the phylogeographic patterns suggest the occurrence of several events of river capture and fauna interchange. The Yaqui River supports the most diverse populations of C. ornatum, with several events of dispersal and isolation within the basin. Based on our genetic results, we defined three ESUs within C. ornatum as a first attempt to promote the conservation of the evolutionary processes determining the genetic diversity of this species. They will likely be revealed as a valuable tool for freshwater conservation policies in northwest Mexico, where many environmental problems concerning the use of water have rapidly arisen in recent decades.
PMCID: PMC3141424  PMID: 21639931
13.  Are Cristaria herculea (Middendorff, 1847) and Cristaria plicata (Leach, 1815) (Bivalvia, Unionidae) separate species? 
ZooKeys  2014;1-15.
The number of species in the freshwater mussel genus Cristaria Schumacher, 1817 recognized from Far East Russia has varied over the last several decades. While some authors consider the occurrence of only one species, Cristaria plicata (Leach, 1815), widespread in East Asia, others, recognize two separate species Cristaria herculea (Middendorff, 1847) and Cristaria tuberculata Schumacher, 1817 from Far East Russia, distinct from C. plicata. For the present study, freshwater mussels, identified as C. herculea, were collected in the Upper Amur basin (Transbaikalia, Russia). The shell morphology and the whole soft body anatomy were analysed in detail and compared with previously published information on other Cristaria spp.. Additionally, a cytochrome oxidase subunit 1 (CO1) gene fragment was sequenced from foot tissue samples of selected animals, collected from the same region, and compared with published data. Based upon morphological similarities of glochidia and adult morphology and anatomy as well as the mitochondrial DNA sequence analysis, we consider C. herculea as a synonym of C. plicata. Further analysis of Far East Russia C. herculea and C. tuberculata specimens using both molecular and morphological characters should be carried in the future to enhance our knowledge about the taxonomy within the Cristaria genus. Moreover, a comprehensive revision of the genus Cristaria is needed, restricting the type locality and comparing topotypic specimens for both C. plicata and C. tuberculata, and including all recognized Cristaria species.
PMCID: PMC4155721  PMID: 25197215
Bivalvia; Unionidae; Anodontini; CO1; Transbaikalia; Russia
14.  Broad-scale sampling of primary freshwater fish populations reveals the role of intrinsic traits, inter-basin connectivity, drainage area and latitude on shaping contemporary patterns of genetic diversity 
PeerJ  2016;4:e1694.
Background. Worldwide predictions suggest that up to 75% of the freshwater fish species occurring in rivers with reduced discharge could be extinct by 2070 due to the combined effect of climate change and water abstraction. The Mediterranean region is considered to be a hotspot of freshwater fish diversity but also one of the regions where the effects of climate change will be more severe. Iberian cyprinids are currently highly endangered, with over 68% of the species raising some level of conservation concern.
Methods. During the FISHATLAS project, the Portuguese hydrographical network was extensively covered (all the 34 river basins and 47 sub-basins) in order to contribute with valuable data on the genetic diversity distribution patterns of native cyprinid species. A total of 188 populations belonging to 16 cyprinid species of Squalius, Luciobarbus, Achondrostoma, Iberochondrostoma, Anaecypris and Pseudochondrostoma were characterized, for a total of 3,678 cytochrome b gene sequences.
Results. When the genetic diversity of these populations was mapped, it highlighted differences among populations from the same species and between species with identical distribution areas. Factors shaping the contemporary patterns of genetic diversity were explored and the results revealed the role of latitude, inter-basin connectivity, migratory behaviour, species maximum size, species range and other species intrinsic traits in determining the genetic diversity of sampled populations. Contrastingly, drainage area and hydrological regime (permanent vs. temporary) seem to have no significant effect on genetic diversity. Species intrinsic traits, maximum size attained, inter-basin connectivity and latitude explained over 30% of the haplotype diversity variance and, generally, the levels of diversity were significantly higher for smaller sized species, from connected and southerly river basins.
Discussion. Targeting multiple co-distributed species of primary freshwater fish allowed us to assess the relative role of historical versus contemporary factors affecting genetic diversity. Since different patterns were detected for species with identical distribution areas we postulate that contemporary determinants of genetic diversity (species’ intrinsic traits and landscape features) must have played a more significant role than historical factors. Implications for conservation in a context of climate change and highly disturbed habitats are detailed, namely the need to focus management and conservation actions on intraspecific genetic data and to frequently conduct combined genetic and demographic surveys.
PMCID: PMC4782715  PMID: 26966653
Cyprinidae; Haplotype diversity; Nucleotide diversity; Mediterranean streams; Freshwater fish conservation; Genetic diversity drivers; Endangered species
15.  Taxonomy and Distribution of Freshwater Pearl Mussels (Unionoida: Margaritiferidae) of the Russian Far East 
PLoS ONE  2015;10(5):e0122408.
The freshwater pearl mussel family Margaritiferidae includes 13 extant species, which are all listed by IUCN as endangered or vulnerable taxa. In this study, an extensive spatial sampling of Margaritifera spp. across the Russian Far East (Amur Basin, Kamchatka Peninsula, Kurile Archipelago and Sakhalin Island) was conducted for a revision of their taxonomy and distribution ranges. Based on their DNA sequences, shell and soft tissue morphology, three valid species were identified: Margaritifera dahurica (Middendorff, 1850), M. laevis (Haas, 1910) and M. middendorffi (Rosén, 1926). M. dahurica ranges across the Amur basin and some of the nearest river systems. M. laevis is distributed in Japan, Sakhalin Island and the Kurile Archipelago. M. middendorffi was previously considered an endemic species of the Kamchatka. However, it is widespread in the rivers of Kamchatka, Sakhalin Island, the Kurile Islands (across the Bussol Strait, which is the most significant biogeographical boundary within the archipelago), and, likely, in Japan. The Japanese species M. togakushiensis Kondo & Kobayashi, 2005 seems to be conspecific with M. middendorffi because of similar morphological patterns, small shell size (<100 mm long) and overlapped ranges, but it is in need of a separate revision. Phylogenetic analysis reveals that two NW Pacific margaritiferid species, M. laevis and M. middendorffi, formed a monophyletic 18S rDNA clade together with the North American species M. marrianae and M. falcata. The patterns that were found in these Margaritifera spp. are similar to those of freshwater fishes, indicating multiple colonizations of Eastern Asia by different mitochondrial lineages, including an ancient Beringian exchange between freshwater faunas across the Pacific.
PMCID: PMC4444039  PMID: 26011762
16.  Freshwater gastropods diversity hotspots: three new species from the Uruguay River (South America) 
PeerJ  2016;4:e2138.
Background: The Atlantic Forest is globally one of the priority ecoregions for biodiversity conservation. In Argentina, it is represented by the Paranense Forest, which covers a vast area of Misiones Province between the Paraná and Uruguay rivers. The Uruguay River is a global hotspot of freshwater gastropod diversity, here mainly represented by Tateidae (genus Potamolithus) and to a lesser extent Chilinidae. The family Chilinidae (Gastropoda, Hygrophila) includes 21 species currently recorded in Argentina, and three species in the Uruguay River. The species of Chilinidae occur in quite different types of habitats, but generally in clean oxygenated water recording variable temperature ranges. Highly oxygenated freshwater environments (waterfalls and rapids) are the most vulnerable continental environments. We provide here novel information on three new species of Chilinidae from environments containing waterfalls and rapids in the Uruguay River malacological province of Argentina.
Materials and Methods: The specimens were collected in 2010. We analyzed shell, radula, and nervous and reproductive systems, and determined the molecular genetics. The genetic distance was calculated for two mitochondrial markers (cytochrome c oxidase subunit I–COI- and cytochrome b -Cyt b-) for these three new species and the species recorded from the Misionerean, Uruguay River and Lower Paraná-Río de la Plata malacological provinces. In addition, the COI data were analyzed phylogenetically by the neighbor-joining and Bayesian inference techniques.
Results: The species described here are different in terms of shell, radula and nervous and reproductive systems, mostly based on the sculpture of the penis sheath. Phylogenetic analyses grouped the three new species with those present in the Lower Paraná-Río de la Plata and Uruguay River malacological provinces.
Discussion: Phylogenetic analyses confirm the separation between the Uruguay River and the Misionerean malacological provinces in northeast Argentina. These new endemic species from the Uruguay River add further support to the suggestion that this river is a diversity hotspot of freshwater gastropods (with 54 species present in this basin, 15 of them endemic). These endemic species from environments with rapids and waterfalls should be taken into account by government agencies before the construction of dams that modify those ecologic niches in the Uruguay River.
PMCID: PMC4911958  PMID: 27326385
Argentina; Chilina luciae sp. nov; Malacological provinces; Chilina nicolasi sp. nov; Chilina santiagoi sp. nov; Conservation; Anatomy
17.  Elevational Gradients in Fish Diversity in the Himalaya: Water Discharge Is the Key Driver of Distribution Patterns 
PLoS ONE  2012;7(9):e46237.
Studying diversity and distribution patterns of species along elevational gradients and understanding drivers behind these patterns is central to macroecology and conservation biology. A number of studies on biogeographic gradients are available for terrestrial ecosystems, but freshwater ecosystems remain largely neglected. In particular, we know very little about the species richness gradients and their drivers in the Himalaya, a global biodiversity hotspot.
Methodology/Principal Findings
We collated taxonomic and distribution data of fish species from 16 freshwater Himalayan rivers and carried out empirical studies on environmental drivers and fish diversity and distribution in the Teesta river (Eastern Himalaya). We examined patterns of fish species richness along the Himalayan elevational gradients (50–3800 m) and sought to understand the drivers behind the emerging patterns. We used generalized linear models (GLM) and generalized additive models (GAM) to examine the richness patterns; GLM was used to investigate relationship between fish species richness and various environmental variables. Regression modelling involved stepwise procedures, including elimination of collinear variables, best model selection, based on the least Akaike’s information criterion (AIC) and the highest percentage of deviance explained (D2). This maiden study on the Himalayan fishes revealed that total and non-endemic fish species richness monotonously decrease with increasing elevation, while endemics peaked around mid elevations (700–1500 m). The best explanatory model (synthetic model) indicated that water discharge is the best predictor of fish species richness patterns in the Himalayan rivers.
This study, carried out along one of the longest bioclimatic elevation gradients of the world, lends support to Rapoport’s elevational rule as opposed to mid domain effect hypothesis. We propose a species-discharge model and contradict species-area model in predicting fish species richness. We suggest that drivers of richness gradients in terrestrial and aquatic ecosystems are likely to be different. These studies are crucial in context of the impacts of unprecedented on-going river regulation on fish diversity and distribution in the Himalaya.
PMCID: PMC3459831  PMID: 23029444
18.  Sources and Delivery of Nutrients to the Northwestern Gulf of Mexico from Streams in the South-Central United States1 
SPAtially Referenced Regressions On Watershed attributes (SPARROW) models were developed to estimate nutrient inputs [total nitrogen (TN) and total phosphorus (TP)] to the northwestern part of the Gulf of Mexico from streams in the South-Central United States (U.S.). This area included drainages of the Lower Mississippi, Arkansas-White-Red, and Texas-Gulf hydrologic regions. The models were standardized to reflect nutrient sources and stream conditions during 2002. Model predictions of nutrient loads (mass per time) and yields (mass per area per time) generally were greatest in streams in the eastern part of the region and along reaches near the Texas and Louisiana shoreline. The Mississippi River and Atchafalaya River watersheds, which drain nearly two-thirds of the conterminous U.S., delivered the largest nutrient loads to the Gulf of Mexico, as expected. However, the three largest delivered TN yields were from the Trinity River/Galveston Bay, Calcasieu River, and Aransas River watersheds, while the three largest delivered TP yields were from the Calcasieu River, Mermentau River, and Trinity River/Galveston Bay watersheds. Model output indicated that the three largest sources of nitrogen from the region were atmospheric deposition (42%), commercial fertilizer (20%), and livestock manure (unconfined, 17%). The three largest sources of phosphorus were commercial fertilizer (28%), urban runoff (23%), and livestock manure (confined and unconfined, 23%).
PMCID: PMC3307634  PMID: 22457582
nutrients; nonpoint source pollution; transport and fate; simulation; watersheds; SPARROW; northwestern Gulf of Mexico; South-Central United States
19.  Redescription of Marstonia comalensis (Pilsbry & Ferriss, 1906), a poorly known and possibly threatened freshwater gastropod from the Edwards Plateau region (Texas) 
ZooKeys  2011;1-16.
Marstonia comalensis, a poorly known nymphophiline gastropod (originally described from Comal Creek, Texas) that has often been confused with Cincinnatia integra, is re-described and the generic placement of this species, which was recently allocated to Marstonia based on unpublished evidence, is confirmed by anatomical study. Marstonia comalensis is a large congener having an ovate-conic, openly umbilicate shell and penis having a short filament and oblique, squarish lobe bearing a narrow gland along its distal edge. It is well differentiated morphologically from congeners having similar shells and penes and is also genetically divergent relative to those congeners that have been sequenced (mtCOI divergence 3.0–8.5%). A Bayesian analysis of a small COI dataset resolved Marstonia comalensis in a poorly supported sub-clade together with Marstonia hershleri, Marstonia lustrica and Marstonia pachyta. The predominantly new records presented herein indicate that Marstonia comalensis was historically distributed in the upper portions of the Brazos, Colorado, Guadalupe and Nueces River basins, south-central Texas. The species has been live collected at only 12 localities and only two of these have been re-visited since 1993. These data suggest that the conservation status of this snail, which has a critically imperiled (G1) NatureServe ranking and was recently proposed for federal listing, needs to be re-assessed.
PMCID: PMC3088054  PMID: 21594148
Marstonia; Hydrobiidae; Gastropoda; United States; Texas; freshwater; taxonomy; conservation
20.  Fish Invasions in the World's River Systems: When Natural Processes Are Blurred by Human Activities  
PLoS Biology  2008;6(2):e28.
Because species invasions are a principal driver of the human-induced biodiversity crisis, the identification of the major determinants of global invasions is a prerequisite for adopting sound conservation policies. Three major hypotheses, which are not necessarily mutually exclusive, have been proposed to explain the establishment of non-native species: the “human activity” hypothesis, which argues that human activities facilitate the establishment of non-native species by disturbing natural landscapes and by increasing propagule pressure; the “biotic resistance” hypothesis, predicting that species-rich communities will readily impede the establishment of non-native species; and the “biotic acceptance” hypothesis, predicting that environmentally suitable habitats for native species are also suitable for non-native species. We tested these hypotheses and report here a global map of fish invasions (i.e., the number of non-native fish species established per river basin) using an original worldwide dataset of freshwater fish occurrences, environmental variables, and human activity indicators for 1,055 river basins covering more than 80% of Earth's surface. First, we identified six major invasion hotspots where non-native species represent more than a quarter of the total number of species. According to the World Conservation Union, these areas are also characterised by the highest proportion of threatened fish species. Second, we show that the human activity indicators account for most of the global variation in non-native species richness, which is highly consistent with the “human activity” hypothesis. In contrast, our results do not provide support for either the “biotic acceptance” or the “biotic resistance” hypothesis. We show that the biogeography of fish invasions matches the geography of human impact at the global scale, which means that natural processes are blurred by human activities in driving fish invasions in the world's river systems. In view of our findings, we fear massive invasions in developing countries with a growing economy as already experienced in developed countries. Anticipating such potential biodiversity threats should therefore be a priority.
Author Summary
As one of the major threats to biodiversity, the detrimental consequences of biological invasions are widely recognised. Despite this, a global view of invasion patterns and their determinants is still lacking in aquatic ecosystems, reducing our ability to initiate practical actions. Here we report the global patterns of freshwater fish invasion in 1,055 river basins covering more than 80% of Earth's continental surface. This allows us to identify six major invasion hotspots where non-native species represent more than a quarter of the total number of species. According to the World Conservation Union, these areas are also characterised by the highest proportion of threatened fish species. We also show that the natural factors controlling global biodiversity do not influence the number of non-native species in a given river basin. Instead, human activity–related factors, and particularly economic activity, explain why some river basins host more non-native species. In view of our findings, we fear massive invasions in developing countries with a growing economy as already experienced in developed countries. This constitutes a serious threat to global biodiversity.
Mapping worldwide freshwater fish invasions allowed the identification of major invasion hot spots and demonstrated that economic activity is the main determinant of freshwater fish invasions at the global scale.
PMCID: PMC2225436  PMID: 18254661
21.  Conservation Genetics of a Critically Endangered Limpet Genus and Rediscovery of an Extinct Species 
PLoS ONE  2011;6(5):e20496.
A third of all known freshwater mollusk extinctions worldwide have occurred within a single medium-sized American drainage. The Mobile River Basin (MRB) of Alabama, a global hotspot of temperate freshwater biodiversity, was intensively industrialized during the 20th century, driving 47 of its 139 endemic mollusk species to extinction. These include the ancylinid limpet Rhodacmea filosa, currently classified as extinct (IUCN Red List), a member of a critically endangered southeastern North American genus reduced to a single known extant population (of R. elatior) in the MRB.
Methodology/Principal Findings
We document here the tripling of known extant populations of this North American limpet genus with the rediscovery of enduring Rhodacmea filosa in a MRB tributary and of R. elatior in its type locality: the Green River, Kentucky, an Ohio River Basin (ORB) tributary. Rhodacmea species are diagnosed using untested conchological traits and we reassessed their systematic and conservation status across both basins using morphometric and genetic characters. Our data corroborated the taxonomic validity of Rhodacmea filosa and we inferred a within-MRB cladogenic origin from a common ancestor bearing the R. elatior shell phenotype. The geographically-isolated MRB and ORB R. elatior populations formed a cryptic species complex: although overlapping morphometrically, they exhibited a pronounced phylogenetic disjunction that greatly exceeded that of within-MRB R. elatior and R. filosa sister species.
Rhodacmea filosa, the type species of the genus, is not extinct. It persists in a Coosa River tributary and morphometric and phylogenetic analyses confirm its taxonomic validity. All three surviving populations of the genus Rhodacmea merit specific status. They collectively contain all known survivors of a phylogenetically highly distinctive North American endemic genus and therefore represent a concentrated fraction of continental freshwater gastropod biodiversity. We recommend the establishment of a proactive targeted conservation program that may include their captive propagation and reintroduction.
PMCID: PMC3105076  PMID: 21655221
22.  The Earliest Post-Paleozoic Freshwater Bivalves Preserved in Coprolites from the Karoo Basin, South Africa 
PLoS ONE  2012;7(2):e30228.
Several clades of bivalve molluscs have invaded freshwaters at various times throughout Phanerozoic history. The most successful freshwater clade in the modern world is the Unionoida. Unionoids arose in the Triassic Period, sometime after the major extinction event at the End-Permian boundary and are now widely distributed across all continents except Antarctica. Until now, no freshwater bivalves of any kind were known to exist in the Early Triassic.
Principal Findings
Here we report on a faunule of two small freshwater bivalve species preserved in vertebrate coprolites from the Olenekian (Lower Triassic) of the Burgersdorp Formation of the Karoo Basin, South Africa. Positive identification of these bivalves is not possible due to the limited material. Nevertheless they do show similarities with Unionoida although they fall below the size range of extant unionoids. Phylogenetic analysis is not possible with such limited material and consequently the assignment remains somewhat speculative.
Bivalve molluscs re-invaded freshwaters soon after the End-Permian extinction event, during the earliest part of the recovery phase during the Olenekian Stage of the Early Triassic. If the specimens do represent unionoids then these Early Triassic examples may be an example of the Lilliput effect. Since the oldest incontrovertible freshwater unionoids are also from sub-Saharan Africa, it is possible that this subcontinent hosted the initial freshwater radiation of the Unionoida. This find also demonstrates the importance of coprolites as microenvironments of exceptional preservation that contain fossils of organisms that would otherwise have left no trace.
PMCID: PMC3271088  PMID: 22319562
23.  Exploratory spatial analysis of Lyme disease in Texas –what can we learn from the reported cases? 
BMC Public Health  2015;15:924.
Lyme disease (LD) is a tick-borne zoonotic illness caused by the bacterium Borrelia burgdorferi. Texas is considered a non-endemic state for LD and the spatial distribution of the state’s reported LD cases is unknown.
We analyzed human LD cases reported to the Texas Department of State Health Services (TX-DSHS) between 2000 and 2011 using exploratory spatial analysis with the objective to investigate the spatial patterns of LD in Texas. Case data were aggregated at the county level, and census data were used as the population at risk. Empirical Bayesian smoothing was performed to stabilize the variance. Global Moran’s I was calculated to assess the presence and type of spatial autocorrelation. Local Indicator of Spatial Association (LISA) was used to determine the location of spatial clusters and outliers.
Results and Discussion
There was significant positive spatial autocorrelation of LD incidence in Texas with Moran’s I of 0.41 (p = 0.001). LISA revealed significant variation in the spatial distribution of human LD in Texas. First, we identified a high-risk cluster in Central Texas, in a region that is thought to be beyond the geographical range of the main vector, Ixodes scapularis. Second, the eastern part of Texas, which is thought to provide the most suitable habitat for I. scapularis, did not appear to be a high-risk area. Third, LD cases were reported from several counties in western Texas, a region considered unsuitable for the survival of Ixodes ticks.
These results emphasize the need for follow-up investigations to determine whether the identified spatial pattern is due to: clustering of misdiagnosed cases, clustering of patients with an out-of state travel history, or presence of a clustered unknown enzootic cycle of B. burgdorferi in Texas. This would enable an improved surveillance and reporting of LD in Texas.
Electronic supplementary material
The online version of this article (doi:10.1186/s12889-015-2286-0) contains supplementary material, which is available to authorized users.
PMCID: PMC4575478  PMID: 26386670
Borrelia burgdorferi; Exploratory spatial data analysis; Lyme disease; Texas
24.  Systematics, conservation and morphology of the spider genus Tayshaneta (Araneae, Leptonetidae) in Central Texas Caves  
ZooKeys  2012;1-102.
The spider genus Tayshaneta is revised based on results from a three gene phylogenetic analysis (Ledford et al. 2011) and a comprehensive morphological survey using scanning electron (SEM) and compound light microscopy. The morphology and relationships within Tayshaneta are discussed and five species-groups are supported by phylogenetic analyses: the anopica group, the coeca group, the myopica group, the microps group and the sandersi group. Short branch lengths within Tayshaneta contrast sharply with the remaining North American genera and are viewed as evidence for a relatively recent radiation of species. Variation in troglomorphic morphology is discussed and compared to patterns found in other Texas cave invertebrates. Several species previously known as single cave endemics have wider ranges than expected, suggesting that some caves are not isolated habitats but instead form part of interconnected karst networks. Distribution maps are compared with karst faunal regions (KFR’s) in Central Texas and the implications for the conservation and recovery of Tayshaneta species are discussed. Ten new species are described: Tayshaneta archambaulti sp. n., Tayshaneta emeraldae sp. n., Tayshaneta fawcetti sp. n., Tayshaneta grubbsi sp. n., Tayshaneta madla sp. n., Tayshaneta oconnorae sp. n., Tayshaneta sandersi sp. n., Tayshaneta sprousei sp. n., Tayshaneta vidrio sp. n. and Tayshaneta whitei sp. n. The males for three species, Tayshaneta anopica (Gertsch, 1974), Tayshaneta devia (Gertsch, 1974) and Tayshaneta microps (Gertsch, 1974) are described for the first time. Tayshaneta furtiva (Gertsch, 1974) and Tayshaneta uvaldea (Gertsch, 1974) are declared nomina dubia as the female holotypes are not diagnosable and efforts to locate specimens at the type localities were unsuccessful. All Tayshaneta species are thoroughly illustrated, diagnosed and keyed. Distribution maps are also provided highlighting areas of taxonomic ambiguity in need of additional sampling.
PMCID: PMC3272638  PMID: 22363201
Spiders; Haplogynae; Leptonetidae; Neoleptoneta, Caves; Endangered Species; Troglobites; Edwards Aquifer; Karst Faunal Regions; Phylogenetics
25.  Phylogeographic Analysis of Blastomyces dermatitidis and Blastomyces gilchristii Reveals an Association with North American Freshwater Drainage Basins 
PLoS ONE  2016;11(7):e0159396.
Blastomyces dermatitidis and Blastomyces gilchristii are dimorphic fungal pathogens that cause serious pulmonary and systemic infections in humans. Although their natural habitat is in the environment, little is known about their specific ecologic niche(s). Here, we analyzed 25 microsatellite loci from 169 strains collected from various regions throughout their known endemic range in North America, representing the largest and most geographically diverse collection of isolates studied to date. Genetic analysis of multilocus microsatellite data divided the strains into four populations of B. dermatitidis and four populations of B. gilchristii. B. dermatitidis isolates were recovered from areas throughout North America, while the B. gilchristii strains were restricted to Canada and some northern US states. Furthermore, the populations of both species were associated with major freshwater drainage basins. The four B. dermatitidis populations were partitioned among (1) the Nelson River drainage basin, (2) the St. Lawrence River and northeast Atlantic Ocean Seaboard drainage basins, (3) the Mississippi River System drainage basin, and (4) the Gulf of Mexico Seaboard and southeast Atlantic Ocean Seaboard drainage basins. A similar partitioning of the B. gilchristii populations was observed among the more northerly drainage basins only. These associations suggest that the ecologic niche where the sexual reproduction, growth, and dispersal of B. dermatitidis and B. gilchristii occur is intimately linked to freshwater systems. For most populations, sexual reproduction was rare enough to produce significant linkage disequilibrium among loci but frequent enough that mating-type idiomorphic ratios were not skewed from 1:1. Furthermore, the evolutionary divergence of B. dermatitidis and B. gilchristii was estimated at 1.9 MYA during the Pleistocene epoch. We suggest that repeated glaciations during the Pleistocene period and resulting biotic refugia may have provided the impetus for speciation as theorized for other species associated with temperate freshwater systems.
PMCID: PMC4948877  PMID: 27428521

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