scholarly journals DNA barcoding in recognition of Gammarusflock diversity and distribution in the ancient Lake Ohrid

2021 ◽  
Vol 4 ◽  
Author(s):  
Anna Wysocka ◽  
Michal Grabowski ◽  
Lidia Sworobowicz ◽  
Sasho Trajanovski ◽  
Tomasz Mamos
Keyword(s):  
Dna Barcoding ◽  
Haplotype Diversity ◽  
Morphological Diversity ◽  
Balkan Peninsula ◽  
Species Flock ◽  
Depth Range ◽  
Ancient Lake ◽  
Lake Ohrid ◽  
Haplotypic Diversity ◽  
Main Driver

Lake Ohrid, located on the Balkan Peninsula at the Albanian-Macedonian border, is the oldest European lake (1.3-1.9 My old) and one of the world’s smallest ancient lakes. Taking into account the size of the lake and its biodiversity, it harbors the highest level of endemism, especially within amphipod crustaceans (ca. 90%) with the endemic Gammarus species flock. Our previous studies upon this flock have shown a substantial decoupling between molecular and morphological diversity, existence of cryptic species and puzzling speciation history. In order to explore sources of observed diversity, in the current study we are investigating ecological preferences of the species within the flock, based on their distribution in depth gradient, in relation to molecular diversity based on DNA barcoding. In the study over 200 barcodes were generated and combined with 173 previously published. The specimens were collected from all depth ranges of Lake Ohrid as well as from springs located on or near the banks of the lake. Within the species flock, 13 BIN’s were identified, 12 previously known and one newly recognized, representing separate lineage and putatively a new species. Two of the flock species were found only in the springs: G. sketi and G. cryptosalemaai. G. sketi, previously found only in springs on the southern banks of Lake Ohrid, has now also been discovered in springs in its north-eastern part. Both species show low haplotypic diversity. All remaining species were recorded from the depth between 20 and 60 meters, that is characterized by the highest ecological diversity with different types of substrates: stones, macrophytes, abundant Dreissena shells as well as sand and silt. Among them G. sywulai, G. macedonicus, G. cryptoparechiniformis, G. lychnidensis, G. ochridensis, G. parechinifromis were found exclusively within this depth range. The three latter species represent single BIN and share haplotypes, at the same time this BIN has the highest number of haplotypes in comparison to others. The remaining species found on this depth represent separate BINs with different levels of haplotype diversity. Only G. lychnidensis, G. stankokaramani and G. solidus were found below the depth of 60 meters, in a quite homogenous environment dominated by silt. In the deepest parts of the lake, between 260 and 290 meters, only G. solidus was found. This species is represented only by three haplotypes while G. stankokaramani is characterized by multiple haplotypes partially shared with G. lychnidensis. The shared haplotype represents the only G. lychnidensis occurrences on the depths below 60 meters. Summarizing, the highest abundance of BINs, species and haplotypes was recovered from the most ecologically diversified depth range of the lake (20 to 60 meters). This suggests that ecological heterogeneity could be the main driver of Gammarus species flock diversification in the ancient Lake Ohrid. Due to the complex pattern of morphological diversity, DNA barcoding proved to be the best if not the only method in identification of the species flock diversity.

scholarly journals Testing the spatial and temporal framework of speciation in an ancient lake species flock: the leech genus <i>Dina</i> (Hirudinea: Erpobdellidae) in Lake Ohrid

2010 ◽  
Vol 7 (11) ◽  
pp. 3387-3402 ◽  
Author(s):  
S. Trajanovski ◽  
C. Albrecht ◽  
K. Schreiber ◽  
R. Schultheiß ◽  
T. Stadler ◽  
...  
Keyword(s):  
Molecular Clock ◽  
Abiotic Factors ◽  
Time Frame ◽  
Recent Common Ancestor ◽  
Species Flock ◽  
Ancient Lake ◽  
Lake Ohrid ◽  
Most Recent Common Ancestor ◽  
Extant Species

Abstract. Ancient Lake Ohrid on the Balkan Peninsula is considered to be the oldest ancient lake in Europe with a suggested Plio-/Pleistocene age. Its exact geological age, however, remains unknown. Therefore, molecular clock data of Lake Ohrid biota may serve as an independent constraint of available geological data, and may thus help to refine age estimates. Such evolutionary data may also help unravel potential biotic and abiotic factors that promote speciation events. Here, mitochondrial sequencing data of one of the largest groups of endemic taxa in the Ohrid watershed, the leech genus Dina, is used to test whether it represents an ancient lake species flock, to study the role of potential horizontal and vertical barriers in the watershed for evolutionary events, to estimate the onset of diversification in this group based on molecular clock analyses, and to compare this data with data from other endemic species for providing an approximate time frame for the origin of Lake Ohrid. Based on the criteria speciosity, monophyly and endemicity, it can be concluded that Dina spp. from the Ohrid watershed, indeed, represents an ancient lake species flock. Lineage sorting of its species, however, does not seem to be complete and/or hybridization may occur. Analyses of population structures of Dina spp. in the Ohrid watershed indicate a horizontal zonation of haplotypes from spring and lake populations, corroborating the role of lake-side springs, particularly the southern feeder springs, for evolutionary processes in endemic Ohrid taxa. Vertical differentiation of lake taxa, however, appears to be limited, though differences between populations from the littoral and the profundal are apparent. Molecular clock analyses indicate that the most recent common ancestor of extant species of this flock is approximately 1.99 ± 0.83 million years (Ma) old, whereas the split of the Ohrid Dina flock from a potential sister taxon outside the lake is estimated at 8.30 ± 3.60 Ma. Comparisons with other groups of endemic Ohrid species indicated that in all cases, diversification within the watershed started ≤2 Ma ago. Thus, this estimate may provide information on a minimum age for the origin of Lake Ohrid. Maximum ages are less consistent and generally less reliable. But cautiously, a maximum age of 3 Ma is suggested. Interestingly, this time frame of approximately 2–3 Ma ago for the origin of Lake Ohrid, generated based on genetic data, well fits the time frame most often used in the literature by geologists.

scholarly journals Testing the spatial and temporal framework of speciation in an ancient lake species flock: the leech genus <i>Dina</i> (Hirudinea: Erpobdellidae) in Lake Ohrid

2010 ◽  
Vol 7 (4) ◽  
pp. 5011-5045 ◽  
Author(s):  
S. Trajanovski ◽  
C. Albrecht ◽  
K. Schreiber ◽  
R. Schultheiß ◽  
T. Stadler ◽  
...  
Keyword(s):  
Molecular Clock ◽  
Abiotic Factors ◽  
Time Frame ◽  
Recent Common Ancestor ◽  
Species Flock ◽  
Ancient Lake ◽  
Lake Ohrid ◽  
Most Recent Common Ancestor ◽  
Extant Species

Abstract. Ancient Lake Ohrid on the Balkan Peninsula is considered to be the oldest ancient lake in Europe with a suggested Plio-Pleistocene age. Its exact geological age, however, remains unknown. Therefore, molecular clock data of Lake Ohrid biota may serve as an independent constraint of available geological data, and may thus also help to refine age estimates. Such evolutionary data may also help unravel potential biotic and abiotic factors that promote speciation events. Here, mitochondrial sequencing data of one of the largest groups of endemic taxa in Lake Ohrid, the leech genus Dina, is used to test whether it represents an ancient lake species flock, to study the role of horizontal and vertical barriers in Lake Ohrid for evolutionary events, to estimate the onset of intralacustrine diversification in this group based on molecular clock analyses, and to compare this data with data from other endemic species for providing an approximate time frame for the origin of Lake Ohrid. Based on the criteria speciosity, monophyly and endemicity, it can be concluded that Lake Ohrid Dina, indeed, represents an ancient lake species flock. Lineage sorting of its species, however, does not seem to be complete. Analyses of population structures of Dina spp. in the Ohrid watershed indicate a horizontal zonation of haplotypes from spring and lake populations, corroborating the role of lake-side springs, particularly the southern feeder springs, for evolutionary processes in endemic Ohrid taxa. Vertical differentiation of lake taxa, however, appears to be limited, though differences between populations from the littoral and the profundal are apparent. Molecular clock analyses indicate that the most recent common ancestor of extant species of this flock is approximately 1.99±0.83 Ma old, whereas the split of the Lake Ohrid Dina flock from a potential sister taxon outside the lake is estimated at 8.30±3.60 Ma. Comparisons with other groups of endemic Ohrid species indicated that in all cases, intralacustrine diversification started ≤2 Ma ago. Thus, this estimate may provide information on a minimum age for the origin of Lake Ohrid. Maximum ages are less consistent and generally less reliable. But cautiously, a maximum age of 3 Ma is suggested. Interestingly, this time frame of approximately 2–3 Ma for the origin of Lake Ohrid, generated based solely on evolutionary data, well fits the time frame most often used in the literature by geologists. Future studies must show whether this concurrence holds true.

scholarly journals Spatially explicit analysis of gastropod biodiversity in ancient Lake Ohrid

2011 ◽  
Vol 8 (1) ◽  
pp. 175-188 ◽  
Author(s):  
T. Hauffe ◽  
C. Albrecht ◽  
K. Schreiber ◽  
K. Birkhofer ◽  
S. Trajanovski ◽  
...  
Keyword(s):  
Environmental Factors ◽  
Water Depth ◽  
Scale Effects ◽  
Small Scale ◽  
Ancient Lakes ◽  
Depth Range ◽  
Ancient Lake ◽  
Lake Ohrid ◽  
Widespread Species ◽  
Neutral Processes

Abstract. The quality of spatial analyses of biodiversity is improved by (i) utilizing study areas with well defined physiogeographical boundaries, (ii) limiting the impact of widespread species, and (iii) using taxa with heterogeneous distributions. These conditions are typically met by ecosystems such as oceanic islands or ancient lakes and their biota. While research on ancient lakes has contributed significantly to our understanding of evolutionary processes, statistically sound studies of spatial variation of extant biodiversity have been hampered by the frequently vast size of ancient lakes, their limited accessibility, and the lack of scientific infrastructure. The European ancient Lake Ohrid provides a rare opportunity for such a reliable spatial study. The comprehensive horizontal and vertical sampling of a species-rich taxon, the Gastropoda, presented here, revealed interesting patterns of biodiversity, which, in part, have not been shown before for other ancient lakes. In a total of 284 samples from 224 different locations throughout the Ohrid Basin, 68 gastropod species, with 50 of them (= 73.5%) being endemic, could be reported. The spatial distribution of these species shows the following characteristics: (i) within Lake Ohrid, the most frequent species are endemic taxa with a wide depth range, (ii) widespread species (i.e. those occurring throughout the Balkans or beyond) are rare and mainly occur in the upper layer of the lake, (iii) while the total number of species decreases with water depth, the proportion of endemics increases, and (iv) the deeper layers of Lake Ohrid appear to have a higher spatial homogeneity of biodiversity. Moreover, gastropod communities of Lake Ohrid and its feeder springs are both distinct from each other and from the surrounding waters. The analysis also shows that community similarity of Lake Ohrid is mainly driven by niche processes (e.g. environmental factors), but also by neutral processes (e.g. dispersal limitation and evolutionary histories of species). For niche-based mechanisms it is shown that large scale effects such as type of water body or water depth are mainly responsible for the similarity of gastropod communities, whereas small scale effects like environmental gradients affect gastropod compositions only marginally. In fact, neutral processes appear to be more important than the small scale environmental factors, thus emphasizing the importance of dispersal capacities and evolutionary histories of species.

scholarly journals Assessing the status of endangered invertebrates from the ancient Lake Ohrid: The gastropod Chilopyrgula sturanyi

2012 ◽  
Vol 64 (2) ◽  
pp. 647-650 ◽  
Author(s):  
Biljana Budzakoska-Gjoreska ◽  
S. Trajanovski ◽  
Sonja Trajanovska
Keyword(s):  
Biological Diversity ◽  
Balkan Peninsula ◽  
Maximum Density ◽  
Northwestern Part ◽  
Ancient Lake ◽  
Lake Ohrid ◽  
Main Subject ◽  
Gastropod Species ◽  
The Status ◽  
High Level

Lake Ohrid is the oldest and deepest lake on the Balkan Peninsula and one of the five oldest lakes in the world. Two of the most striking attributes of the species of the Lake?s fauna, especially the fauna of gastropods, are the high level of biological diversity as well as a high percentage of endemism. The main subject of interest in our research was to follow the distribution and density of the endemic gastropod species Chilopyrgula sturanyi. For this purpose different depth points of the transect Hydrobiological Institute-Radozda as well as other littoral points on the northwestern part of Lake Ohrid, were investigated. The results showed maximum density in the population of Chilopyrgula sturanyi in the muddy lakebed covered by Chara tomentosa. The minimum density in population was recorded on the lakebed with gravel. Specimens of Chilopyrgula sturanyi were not recorded at the depth of 50 m, where the lakebed is covered by a sandy-muddy substrate.

Rapid evolution of an ancient lake species flock: Freshwater limpets (Gastropoda: Ancylidae) in the Balkan Lake Ohrid

2006 ◽  
Vol 6 (4) ◽  
pp. 294-307 ◽  
Author(s):  
C ALBRECHT ◽  
S TRAJANOVSKI ◽  
K KUHN ◽  
B STREIT ◽  
T WILKE
Keyword(s):  
Rapid Evolution ◽  
Species Flock ◽  
Ancient Lake ◽  
Lake Ohrid

А new species of Alona Baird, 1843 (Cladocera: Chydoridae) from the ancient Lake Ohrid

Zootaxa ◽  
2018 ◽  
Vol 4526 (4) ◽  
pp. 434
Author(s):  
ARTEM Y. SINEV ◽  
CHARO LÓPEZ-BLANCO
Keyword(s):  
New Species ◽  
Ancient Lakes ◽  
Ancient Lake ◽  
Lake Ohrid ◽  
Genus Level ◽  
Palearctic Species ◽  
Level Group ◽  
A New Species

A new species of Cladocera, Alona begoniae sp. nov. (Anomopoda: Chydoridae) was found in ancient Lake Ohrid. Its habitus and outer morphology is similar to one of the most common Palearctic species, Coronatella rectangula (Sars, 1862), and this can be the main reason why it has remained undiscovered. A. begoniae sp. nov. belongs to the elegans-group of Alona s. lato, a relict genus-level group not formally recognised yet as a separate taxonomical unit. Its habitat seem to be sandy and stony substrates (at 2–12 m depth) bare of vegetation. The position of this new species within the Alona-like anomopods is evaluated and similarities with other cladocerans in ancient lakes are discussed. 

scholarly journals Assembly processes of gastropod community change with horizontal and vertical zonation in ancient Lake Ohrid: a metacommunity speciation perspective

2016 ◽  
Vol 13 (10) ◽  
pp. 2901-2911 ◽  
Author(s):  
Torsten Hauffe ◽  
Christian Albrecht ◽  
Thomas Wilke
Keyword(s):  
Community Composition ◽  
Community Assembly ◽  
Environmental Filtering ◽  
Dispersal Limitation ◽  
Species Interaction ◽  
Relative Importance ◽  
Lake Depth ◽  
Ancient Lake ◽  
Lake Ohrid ◽  
Speciation Model

Abstract. The Balkan Lake Ohrid is the oldest and most diverse freshwater lacustrine system in Europe. However, it remains unclear whether species community composition, as well as the diversification of its endemic taxa, is mainly driven by dispersal limitation, environmental filtering, or species interaction. This calls for a holistic perspective involving both evolutionary processes and ecological dynamics, as provided by the unifying framework of the “metacommunity speciation model”.The current study used the species-rich model taxon Gastropoda to assess how extant communities in Lake Ohrid are structured by performing process-based metacommunity analyses. Specifically, the study aimed (1) to identifying the relative importance of the three community assembly processes and (2) to test whether the importance of these individual processes changes gradually with lake depth or discontinuously with eco-zone shifts.Based on automated eco-zone detection and process-specific simulation steps, we demonstrated that dispersal limitation had the strongest influence on gastropod community composition. However, it was not the exclusive assembly process, but acted together with the other two processes – environmental filtering and species interaction. The relative importance of the community assembly processes varied both with lake depth and eco-zones, though the processes were better predicted by the latter.This suggests that environmental characteristics have a pronounced effect on shaping gastropod communities via assembly processes. Moreover, the study corroborated the high importance of dispersal limitation for both maintaining species richness in Lake Ohrid (through its impact on community composition) and generating endemic biodiversity (via its influence on diversification processes). However, according to the metacommunity speciation model, the inferred importance of environmental filtering and biotic interaction also suggests a small but significant influence of ecological speciation. These findings contribute to the main goal of the Scientific Collaboration on Past Speciation Conditions in Lake Ohrid (SCOPSCO) deep drilling initiative – inferring the drivers of biotic evolution – and might provide an integrative perspective on biological and limnological dynamics in ancient Lake Ohrid.

scholarly journals Sediment core fossils in ancient Lake Ohrid: testing for faunal change in molluscs since the Last Interglacial period

2010 ◽  
Vol 7 (3) ◽  
pp. 3969-3999 ◽  
Author(s):  
C. Albrecht ◽  
H. Vogel ◽  
T. Hauffe ◽  
T. Wilke
Keyword(s):  
Sediment Core ◽  
Fossil Record ◽  
Interglacial Period ◽  
Ancient Lake ◽  
Last Interglacial ◽  
Lake Ohrid ◽  
Last Interglacial Period ◽  
History Of ◽  
Extinction Events ◽  
Mollusc Shells

Abstract. Ancient Lake Ohrid is probably of early Pleistocene or Pliocene origin and amongst the few lakes in the world harboring an outstanding degree of endemic biodiversity. Although there is a long history of evolutionary research in Lake Ohrid, particularly on molluscs, a mollusc fossil record has been missing up to date. For the first time, gastropod and bivalve fossils are reported from the basal, calcareous part of a 2.6 m long sediment succession (core Co1200) from the north-eastern part of Lake Ohrid. Electron spin resonance (ESR) dating of mollusc shells from the same stratigraphic level yielded an age of 130±28 ka. Lithofacies III sediments, i.e. a subdivision of the stratigraphic unit comprising the basal succession of core Co1200 between 181.5–263 cm appeared solid, grayish-white, and consisted almost entirely of silt-sized endogenic calcite (CaCO3>70%) and intact and broken mollusc shells. Here we compare the faunal composition of the thanatocoenosis with recent mollusc associations in Lake Ohrid. A total of 13 mollusc species (9 gastropod and 4 bivalve species) could be identified within Lithofacies III sediments. The value of sediment core fossils for reconstructing palaeoenvironmental settings was evaluated. The agreement between sediment and palaeontological proxies was tested. The combined findings of the ecological study and the sediment characteristics suggest deposition in a shallow water environment during the Last Interglacial period. We tested for major faunal changes since the Last Interglacial period and searched for signs of extinction events. The fossil fauna exclusively included species also found in the present fauna, i.e. no extinction events are evident for this site since the Last Interglacial. The thanatocoenosis showed the highest similarity with recent Intermediate Layer (5–25 m) mollusc assemblages. The demonstrated existence of a mollusc fossil record in Lake Ohrid sediment cores also has great significance for future deep drilling projects. It can be hoped that a more far reaching mollusc fossil record will then be obtained, enabling insight into the early evolutionary history of Lake Ohrid.

scholarly journals Differential resilience of ancient sister lakes Ohrid and Prespa to environmental disturbances during the Late Pleistocene

2015 ◽  
Vol 12 (18) ◽  
pp. 16049-16079 ◽  
Author(s):  
E. Jovanovska ◽  
A. Cvetkoska ◽  
T. Hauffe ◽  
Z. Levkov ◽  
B. Wagner ◽  
...  
Keyword(s):  
Late Pleistocene ◽  
Sediment Cores ◽  
Balkan Peninsula ◽  
Model Systems ◽  
Campi Flegrei ◽  
Tephra Layer ◽  
Diatom Community ◽  
Lake Ohrid ◽  
Environmental Disturbances ◽  
Lake Prespa

Abstract. Ancient lakes, like lakes Ohrid and Prespa on the Balkan Peninsula, have become model systems for studying the link between geological and biotic evolution. Recently the scientific deep drilling program "Scientific Collaboration on Past Speciation Conditions in Lake Ohrid" (SCOPSCO) has been launched to better understand the environmental, climatic and limnological evolution of the lake. It revealed that Lake Ohrid experienced a number of environmental disturbances during its ca. 2.0 million year long history. They comprise disturbances that lasted over longer periods of times ("press events") such as Heinrich events as well as sudden and short disturbances ("pulse events") like the deposition of volcanic ashes. The latter include one of the most severe volcanic episodes during the Late Pleistocene, the eruption of the Campanian Ignimbrite (known as Y-5 marine tephra layer) from the Campi Flegrei caldera, dated at 39.6 ± 0.1 ka ago. The event is recorded by the deposition of a ca. 15 cm thick Y-5 tephra layer in sediment cores of lakes Ohrid (DEEP-5045-1) and Prespa (Co1204). This pulse event is overlain by the Heinrich event 4 (H4), 40.0–38.0 ka ago. In the current paper, diatoms were used as proxies to compare the responses of these lakes to the Y-5 (pulse) and the H4 (press) disturbances. Based on stratigraphically constrained incremental sum of squares cluster (CONISS) and unconstrained Partitioning Around Medoids (PAM) analyses, we found only little evidence that the diatom community compositions in either lake responded to the H4 event. However, the Y-5 influx caused clear and rapid diatom community changes. After the initial response, community composition in Lake Ohrid and, to a lesser extent, in Lake Prespa slowly returned to their quasi pre-disturbance state. Moreover, there is no evidence for disturbance-related extinction events. The combined evidence from these findings suggests that lakes Ohrid and Prespa likely did not experience regime shifts. It is therefore concluded that both lakes show resilience to environmental disturbance. However, it seems that Lake Ohrid is more resilient than Lake Prespa as the recovery of diatom communities is more pronounced and as its estimated recovery time is only ca. 1400 years vs. ca. 3600 years in Lake Prespa. The reasons for the differential responses remain largely unknown, but differences in geology, lake age, limnology, and intrinsic parameters of the diatom proxies may play a role. Given the relative robust results obtained, this study provides important new insights into the response of lakes to (multiple) environmental disturbances. Moreover, it contributes to one of the major goals of the SCOPSCO project – to evaluate the influence of major geological events onto the evolution of endemic taxa in Lake Ohrid.

Sign in / Sign up

Export Citation Format

Share Document