Deep drilling reveals massive shifts in evolutionary dynamics after formation of ancient ecosystem

The scarcity of high-resolution empirical data directly tracking diversity over time limits our understanding of speciation and extinction dynamics and the drivers of rate changes. Here, we analyze a continuous species-level fossil record of endemic diatoms from ancient Lake Ohrid, along with environmental and climate indicator time series since lake formation 1.36 million years (Ma) ago. We show that speciation and extinction rates nearly simultaneously decreased in the environmentally dynamic phase after ecosystem formation and stabilized after deep-water conditions established in Lake Ohrid. As the lake deepens, we also see a switch in the macroevolutionary trade-off, resulting in a transition from a volatile assemblage of short-lived endemic species to a stable community of long-lived species. Our results emphasize the importance of the interplay between environmental/climate change, ecosystem stability, and environmental limits to diversity for diversification processes. The study also provides a new understanding of evolutionary dynamics in long-lived ecosystems.

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Constant diversification rates of endemic gastropods in ancient Lake Ohrid: ecosystem resilience likely buffers environmental fluctuations

Biogeosciences ◽

10.5194/bg-12-7209-2015 ◽

2015 ◽

Vol 12 (23) ◽

pp. 7209-7222 ◽

Cited By ~ 24

Author(s):

K. Föller ◽

B. Stelbrink ◽

T. Hauffe ◽

C. Albrecht ◽

T. Wilke

Keyword(s):

Diversification Rate ◽

Ancient Lakes ◽

Freshwater Species ◽

Ecosystem Resilience ◽

Ancient Lake ◽

Lake Ohrid ◽

Deep Drilling ◽

Diversification Rates ◽

Environmental Events ◽

Over Time

Abstract. Ancient lakes represent key ecosystems for endemic freshwater species. This high endemic biodiversity has been shown to be mainly the result of intra-lacustrine diversification. Whereas the principle role of this mode of diversification is generally acknowledged, actual diversification rates in ancient lakes remain little understood. At least four types are conceivable. Diversification rates may be constant over time, they may fluctuate, rates may be higher in the initial phase of diversification, or there may be a pronounced lag phase between colonization and subsequent diversification. As understanding the tempo of diversification in ancient lake environments may help reveal the underlying processes that drive speciation and extinction, we here use the Balkan Lake Ohrid as a model system and the largest species flock in the lake, the non-pyrgulinid Hydrobiidae, as a model taxon to study changes in diversification rates over time together with the respective drivers. Based on phylogenetic, molecular-clock, lineage-through-time plot, and diversification-rate analyses we found that this potentially monophyletic group is comparatively old and that it most likely evolved with a constant diversification rate. Preliminary data of the SCOPSCO (Scientific Collaboration On Past Speciation Conditions in Lake Ohrid) deep-drilling program do indicate signatures of severe environmental/climatic perturbations in Lake Ohrid. However, so far there is no evidence for the occurrence of catastrophic environmental events. We therefore propose that the constant diversification rate observed in endemic gastropods has been caused by two factors: (i) a potential lack of catastrophic environmental events in Lake Ohrid and/or (ii) a probably high ecosystem resilience, buffering environmental changes. Parameters potentially contributing to the lake's high ecosystem resilience are its distinct bathymetry, ongoing tectonic activities, and karst hydrology. The current study not only contributes to one of the overall goals of the SCOPSCO deep-drilling program – inferring the driving forces for biotic evolution in Lake Ohrid. It might also enhance our understanding of how ecosystem resilience, in general, may promote relatively constant diversification rates in isolated ecosystems. However, we encourage future studies testing hypotheses about the lack of catastrophic events in Lake Ohrid. These studies should be based on high-resolution data for the entire geological history of the lake, and they should potentially involve information from the sediment fossil record, not only for gastropods but also for other groups with a high share of endemic taxa.

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Constant diversification rates of endemic gastropods in ancient Lake Ohrid: ecosystem resilience likely buffers environmental fluctuations

Biogeosciences Discussions ◽

10.5194/bgd-12-14271-2015 ◽

2015 ◽

Vol 12 (16) ◽

pp. 14271-14302 ◽

Cited By ~ 4

Author(s):

K. Föller ◽

B. Stelbrink ◽

T. Hauffe ◽

C. Albrecht ◽

T. Wilke

Keyword(s):

Diversification Rate ◽

Ancient Lakes ◽

Freshwater Species ◽

Ecosystem Resilience ◽

Ancient Lake ◽

Lake Ohrid ◽

Deep Drilling ◽

Diversification Rates ◽

Environmental Events ◽

Over Time

Abstract. Ancient lakes represent key ecosystems for endemic freshwater species. This high endemic biodiversity has been shown to be mainly the result of intra-lacustrine diversification. Whereas the principle role of this mode of diversification is generally acknowledged, actual diversification rates in ancient lakes remain little understood. At least four modes are conceivable. Diversification rates may be constant over time, they may fluctuate, rates may be higher in the initial phase of diversification, or there may be a pronounced lag phase between colonization and subsequent diversification. As understanding the tempo of diversification in ancient lake environments may help unrevealing the underlying processes that drive speciation and extinction, we here use the Balkan Lake Ohrid as a model system and the largest species flock in the lake, the non-pyrgulinid Hydrobiidae, as a model taxon to study changes in diversification rates over time together with the respective drivers. Based on phylogenetic, molecular-clock, lineage-through-time plot and diversification-rate analyses we found that this monophyletic group is comparatively old and that it most likely evolved with a constant diversification rate. Preliminary data of the SCOPSCO deep-drilling program do indicate signatures of severe environmental/climatic perturbations in Lake Ohrid. However, so far there is no evidence for the occurrence of catastrophic environmental events. We therefore propose that the rate homogeneity observed in endemic gastropods has been caused by two factors: (i) a potential lack of catastrophic environmental events in Lake Ohrid and/or (ii) a high ecosystem resilience, buffering environmental changes. Parameters potentially contributing to the lake's high ecosystem resilience are its distinct bathymetry, ongoing tectonic activities, and karst hydrology. The current study not only contributes to one of the overall goals of the SCOPSCO deep-drilling program – inferring the driving forces for biotic evolution in Lake Ohrid. It might also enhance our understanding of how ecosystem resilience, in general, may promote relative constant diversification rates in isolated ecosystems. However, we encourage future studies testing hypotheses about the lack of catastrophic events in Lake Ohrid. These studies should be based on high-resolution data for the entire geological history of the lake, and potentially involving information from the sediment fossil record, not only for gastropods but also for other groups with a high share of endemic taxa.

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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

Biogeosciences ◽

10.5194/bg-7-3387-2010 ◽

2010 ◽

Vol 7 (11) ◽

pp. 3387-3402 ◽

Cited By ~ 32

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.

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

Zootaxa ◽

10.11646/zootaxa.4526.4.2 ◽

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.

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

Biogeosciences ◽

10.5194/bg-13-2901-2016 ◽

2016 ◽

Vol 13 (10) ◽

pp. 2901-2911 ◽

Cited By ~ 9

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.

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

Biogeosciences Discussions ◽

10.5194/bgd-7-3969-2010 ◽

2010 ◽

Vol 7 (3) ◽

pp. 3969-3999 ◽

Cited By ~ 3

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.

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

ARPHA Conference Abstracts ◽

10.3897/aca.4.e65011 ◽

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.

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Surirella subrotunda sp. nov. and Surirella parahelvetica sp. nov., two new diatom (Bacillariophyta) species from Lake Prespa, Macedonia

Phytotaxa ◽

10.11646/phytotaxa.156.3.5 ◽

2014 ◽

Vol 156 (3) ◽

pp. 145 ◽

Cited By ~ 1

Author(s):

ALEKSANDRA CVETKOSKA ◽

ZLATKO LEVKOV ◽

PAUL B. HAMILTON

Keyword(s):

Ancient Lakes ◽

Similar Species ◽

Ancient Lake ◽

Lake Ohrid ◽

Fossil Species ◽

Size And Shape ◽

Lake Prespa ◽

Median Area

The genus Surirella is highly diverse and many taxa are reported as endemic, especially from ancient lakes and tropical continental regions. In ancient Lake Ohrid, 25 different Surirella species have been identified by different authors, five are considered to be endemic for the lake. In contrast, research on its sister Lake Prespa has been less rigorous and data for recent and fossil species of Surirella is very sparse. The number of Surirella taxa reported from Lake Prespa is 11; only one is considered an endemic for both lakes, Ohrid and Prespa. In this study, taxa from the genus Surirella were observed in a number of recent and fossil samples from Lake Prespa. Two taxa possess unique characters that distinguish them from known species. Their formal descriptions, based on detailed LM and SEM observations, are presented here. Surirella subrotunda sp. nov. is differentiated from other similar species by its valve outline, size, and shape of median area; it has been observed only in fossil diatom samples from core Co1215 recovered from Lake Prespa. Surirella parahelvetica sp. nov. is distinguished by its size, valve outline, number of alar canals and stria density.

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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

Biogeosciences Discussions ◽

10.5194/bgd-7-5011-2010 ◽

2010 ◽

Vol 7 (4) ◽

pp. 5011-5045 ◽

Cited By ~ 6

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.

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On the Banks of an Ancient Lake

Peacemakers ◽

10.5810/kentucky/9780813174358.003.0031 ◽

2018 ◽

Author(s):

James W. Pardew

Keyword(s):

Civil War ◽

Ancient Lake ◽

Lake Ohrid

The talks resolve most issues after the talks move to the shore of Lake Ohrid. But the execution of NLA fighters and the ambush of a Macedonian Army convoy threaten to destroy the negotiations. President Trajkovski steps in to complete the agreement and prevent a destructive civil war. NATO then moves to disarm the NLA.

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