Australia: The Land Where Time Began
Massive Shifts in Evolutionary Dynamics Following Formation of Ancient Ecosystem Revealed by Deep Drilling
Understanding of speciation and extinction dynamics and the drivers of rate changes is limited by the scarcity of high resolution empirical data that tracks diversity over time. In this study a continuous species level record of endemic diatoms from ancient Lake Ohrid were analysed, as well as environmental and climate indicator time series since the formation of the lake 1.36 million years ago (Ma). Speciation and rates of extinction decreased nearly simultaneously in the environmentally dynamic phase following the formation of the ecosystem which became stabilised after deep water conditions became established in Lake Ohrid. There was also a switch to the macroevolutionary trade-off as the lake deepened, which resulted in a transition to a volatile assemblage of endemic species that were short lived to a stable community 0f long-lived species. The importance of the interplay between environmental/climate change, ecosystem stability, and environmental limits to diversity for diversification processes are emphasised by the results of this study. A new understanding of evolutionary dynamics in ecosystems that are long-lived is also provided by this study.
Lake Ohrid (Republic of Albania/Republic of North Macedonia; 40o54’N to 41o10’N to 20o37’N to 20o48’E; 603 m above sea level) tectonically formed the oligotrophic lake that has a tub-shaped morphology. It is about 30 km long, 15 km wide, and its maximum water depth is 293 m (Lindhorst et al., 2015). Input of water is from karst springs (64%) and from direct precipitation and river inflow (36%) (Lacey & Jones, 2018). During the Miocene the Ohrid Basin was formed by transtension and opened during the Pliocene and Pleistocene (Wagner et al., 2017). Sediments of various types were deposited until 1.36 Ma (Lacey & Jones, 2018), Peat, slack water, and fluvial, following which continuous hemipelagic sedimentation began (i.e., the formation of Lake Ohrid of the present) (Wagner et al., 2019). Deepening and widening is indicated during an early extensional phase of development of the lake basin by a shift to higher lake water oxygen isotope values δ18Oslakwater) and a decrease in grain size 1.36 to 1.15 Ma (Panagiotoulos et al., 2020; Lindhorst et al., 2015). It is indicated by the absence of truncations in seismic reflection data (Lindhorst et al., 2015), together with the absence of shallow-water deposits in the drill core records (Wagner et al., 2017), that no desiccation has occurred since the formation of the lake 1.36 Ma,
At present the lake fills almost the entire basin, as a result of the narrow shape of the basin, and the watershed size is comparably small. There is a considerable degree of in situ speciation among diatoms, as a result of the relative isolation of the lake, in combination with its high age (Stelbrink et al., 2018). Lake Baikal is the only other place that is known of where there is a similar level of diatom diversity, which, however, has an area that is 2 orders of magnitude larger than Lake Ohrid.
What determines the diversity of species is one of the fundamental questions in biology (Benton, 2016). Diversification is defined by macroevolutionary theory as interplay between speciation and extinction (Simpson, 1953; Schluter, 2000). Conceptional models for isolated ecosystems assume that the interplay and the accumulation of in situ species diversity over time typically lead to a flattening of the species accumulation curve and (a dynamic equilibrium diversity [e.g., the general dynamic model of isolated biogeography (Whittaker, Triantis & Ladle, 2008), the unified neutral theory of biodiversity and biogeography (Hubbell, 2001), the concept of ecological opportunity, and the concept of equilibrium speciation dynamics (Rabosky & Glor, 2010)]. It is typically assumed by these conceptual diversification models that increasing competition, decreasing range of population sizes, and/or the decreasing of niches with increasing species richness (Whittaker, Triantis & Ladle, 2008; Rosindell & Phillimore, 2011). As the result of scarcity of empirical data that track directly the biodiversity and environmental change over time, there is only limited understanding of actual speciation and extinction trajectory and the biotic and abiotic drivers of diversification. There are 5 empirical challenges:
1. There are only a few study systems have persisted over time scales that are evolutionarily relevant, and that have a sufficient number of endemic species to enable analysis of in situ diversification processes.
2. Within the fossil record uneven representation (Smiley, 2018) and inherent difficulties in quantifying extinction from molecular phylogenies (Quental & Maxwell, 2010; Louca & Pennell, 2020), hampers precise estimation of species and rates of extinction.
3. Local environmental time series that cover the entire history of an isolated ecosystem, and are dated reliably, are scarce, which makes it difficult to infer the drivers of evolutionary dynamics.
These challenges are met by Lake Ohrid, which is the most species-rich freshwater lake (Albrecht & Wilke, 2008) in Europe. The lake has existed continuously for 1.36 million years (Myr) (Wagner et al., 2019). Bacillariophyta, diatoms, are the most biodiverse group in the lake. They are from 2 subphyla Coscinodiscophytina (Panayiotopoulos et al., 2020) species and Bacillariophytina (184 species) which represent mainly planktonic and benthic lifestyles in Lake Ohrid, respectively. In the lake both groups are paraphyletic, and there is preliminary evidence of both anagenetic and cladogenetic speciation (Stelbrink et al., 2018). The vast majority of endemic benthic species are present in small populations that are restricted to the southern and eastern parts of the lake (Cvetkoska et al., 2018). They inhabit the photic zone, which extends to a depth of about 80 m in Lake Ohrid, as diatoms are autotrophic organisms (Albrecht & Wilke, 2008). Diatoms are a key taxon for palaeoenvironmental reconstructions from lake sediments, as well as for unravelling evolutionary dynamics through time, because the silica shells (“frustules”) of these primary producers may form microfossil successions (Cohen, 2003).
In 2013 a continuous sediment succession was obtained from Lake Ohrid as part of the international Continental Scientific Drilling Program (ICDP). The upper 447 m of the composite record comprise lacustrine sediments that had been deposited continuously since the formation of the lake 1.36 Ma (Wagner et al., 2019). They are comprised of the environmentally dynamic shallow water (1.36 to 1.15 Ma) as well as the deep water phases that are the phases that are more stable (1.15 to 0 Ma) (Wagner, 2019; Panagiotopoulos et al., 2020). Uninterrupted environmental and climate indicator time series and a unique record of diatom species at a sample resolution of around 20,000 to 4,000 years, resulted from processing of the core. The sequence comprises 75.6% of all endemic species of diatoms that have ever been found in the lake, with a total of 152 to 201 of a total of diatom species that were recovered.
In this study, the speciation and extinction dynamics of Lake Ohrid’s endemic diatom assemblage since the formation of this ancient ecosystem 1.36 Ma was assessed, and an explanation is offered for the temporal changes in rates of diversification and the underlying drivers of evolutionary dynamics.
Evolutionary rates decrease simultaneously with deepening of the lake
The pattern of accumulation of endemic species in Lake Ohrid is shown by the data from this study to be consistent with conceptual diversification models that are applicable to insular ecosystems, which display a diversity buildup deceleration over time and with increasing diversity (Whittaker, Triantis & Ladle, 2008; Hubbell, 2001; Rosindell & Phillimore, 2011). In this study it was found, however, that the extinction rate per lineage decreased during the early phase of Lake Ohrid, as opposed to an increasing extinction rate that is suggested by these models.
Wilke et al. suggested that the ample ecological opportunity (Schluter, 2000; Wellborn & Langerhans, 2015) encountered by the diatom species that colonised the emerging lake 1.36 Ma facilitated diversification which initially led to a high rate of speciation. Simultaneously, the habitable space that was relatively small together with high environmental dynamics (Panagiotopoulos et al., 2020) was the likely cause of the frequent extinctions of endemic species. The high rate of speciation declined as the lake expanded and deepened, probably as a result of a negative effect, that was increasing, of the diversity dependence when species richness approached the limit to diversity defined by the size of the lake.
A time-lagged decrease in the rate of extinction accompanied the decline in the rate of speciation that was observed. Wilke et al. suggested that the latter was likely to be due to the increasing environmental and microclimate buffering sensu (O’Sullivan & Reynolds, 2008; Barry & Blanken, 2016) in the deepening lake. Moreover, larger sizes of the population was likely to be supported by the rapid expansion of habitable space, as was suggested by the negative effect of lake size indicators on the extinction rate. During the shallow water phase of Lake Ohrid the expected longevity of endemic species of diatoms was comparatively low, though it increased rapidly with the expansion of the lake. These changes were not significant, as indicated by the lack of shifts in extinction rate during the 1.2 Myr, and values remained largely within the range reported for freshwater diatoms globally, though the longevity varied following the deepening of the lake. This is probably a result of Lake Ohrid’s environmental and microclimate buffering during deep-water conditions.
From volatility to stability
In the diatoms of Lake Ohrid the trajectories of evolutionary rates points to a macroevolutionary trade off, i.e., rates of speciation and extinction are not independent and so covary loosely (Jablonski, 2013). Moreover, there is a switch in the macroevolutionary trade-off from “increaser” taxa – constituent species with high rates of speciation and short longevities – to “survivor” taxa – species with low rates of speciation and high longevities sensu (Jablonski, 2017). Increaser taxa are more likely to be more susceptible to stochastic effects and external perturbations, which makes these volatile species more likely to disappear, while the 2 types may represent equivalent strategies with theoretically similar risks of extinction (Jablonski, 2017). The high initial speciation and extinction rates support this assumption of a switch in the macroevolutionary trade-off in Lake Ohrid diatoms, the nonindependence of these rates over time, the selective extinction in some clades, and the increasing environmental dependence of the speciation rate. Moreover, there was a decrease over time in the mean pairwise taxonomic distance of the endemic diatom assemblage. An increasing invasibility of Lake Ohrid by species that were not endemic was observed, which reflected the decreasing rate of immigration. Together with a decreasing (local) rate of extinction, this resulted in longer persistence of nonendemic diatoms in the lake. It is indicated by these findings that an increasing coexistence of constituent taxa, which led to a rich and stable community sensu (Serván et al., 2018).
Combining the results of the diversification rate and environmental correlate analysis of Wilke et al., they hypothesised that a volatile assemblage of diatom species that were short lived, which encountered ecological opportunity in the developing ecosystem, evolved into a stable community of endemic species that were long-lived after the lake had achieved long-term stability. The important role of:
i) Ecosystem buffering for mitigating the effects of environmental and climate dynamics on diversification processes, and
ii) Environmentally defined ecological limits to diversity in isolated ecosystems.
Not all taxa respond equally
Selective extinction that has been observed within the small planktonic subphylum Coscinodiscophytina, e.g., indicates the high evolutionary volatility of this clade, though it has been shown by the analyses in this study there is an overall decreasing extinction rate in the diatom community of Lake Ohrid over time. Most of the members of this clade prefer conditions that are nutrient-rich, which was assumed by Wilke et al. was the case for the shallow-water phase of the lake (Panagiotopoulos et al., 2020). The conditions became more oligotrophic as the lake deepened (Panagiotopoulos, 2020), and at this point of the history of the lake many Coscinodiscophytina species became extinct, probably as they weren’t capable of withstanding the reduced levels of nutrients. The subphylum Bacillariophytina, in contrast, continued proliferating, and this resulted in an outstanding diversity of 184 extant endemic species.
The reason for the relative volatility of the Coscinodiscophytina in Lake Ohrid is not known, and, with only 17 species, the species number of Coscinodiscophytina is not large enough to allow meaningful analyses of diversification rates and environmental correlates. Nevertheless, Wilke et al. proposed the hypothesis of trait-based selective extinction in this high-nutrient-dependent “increaser” clade.
The value of high-resolution empirical data
In this paper Wilke et al. provided an unprecedented view of in situ diversification in an ancient ecosystem and show that during the early phase of the formation of ecosystem short-term environmental changes have strong effects on macroevolutionary dynamics and dynamics and long-term buildup of diversity.
Their results therefore emphasise the importance of fossil and environmental time series for a comprehensive assessment of speciation and extinction dynamics (Louca & Pennell, 2020). Because the temporal resolution of their study has to date not been matched by molecular phylogenetics, their findings have provided a unique contribution to the understanding of temporal evolutionary dynamics in long-lived ecosystems. They may also server as a baseline for future explorations of adaptive radiations, which often arise from ecological opportunity (Shluter, 2000; Wellborn & Langerhans, 2000).
Wilke, T., et al. (2020). "Deep drilling reveals massive shifts in evolutionary dynamics after formation of ancient ecosystem." Science Advances 6(40): eabb2943.
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