Michal Kucera

The cryptic and the apparent reversed: lack of genetic differentiation within the morphologically diverse plexus of the planktonic foraminifer Globigerinoides sacculifer

Abstract Previous genetic studies of extant planktonic foraminifera have provided evidence that the traditional, strictly morphological definition of species in these organisms underestimates their biodiversity. Here, we report the first case where this pattern is reversed. The modern (sub)tropical species plexus Globigerinoides sacculifer is characterized by large morphological variability, which has led to the proliferation of taxonomic names attributed to morphological end-members within the plexus. In order to clarify the taxonomic status of its morphotypes and to investigate the genetic connectivity among its currently partly disjunct (sub)tropical populations, we carried out a global survey of two ribosomal RNA regions (SSU and ITS-1) in all recent morphotypes of the plexus collected throughout (sub)tropical surface waters of the global ocean. Unexpectedly, we find an extremely reduced genetic variation within the plexus and no correlation between genetic and morphological divergence, suggesting taxonomical overinterpretation. The genetic homogeneity within the morphospecies is unexpected, considering its partly disjunct range in the (sub)tropical Atlantic and Indo-Pacific and its old age (early Miocene). A sequence variant in the rapidly evolving ITS-1 region indicates the existence of an exclusively Atlantic haplotype, which suggests an episode of relatively recent (last glacial) isolation, followed by subsequent resumption of unidirectional gene flow from the Indo-Pacific into the Atlantic. This is the first example in planktonic foraminifera where the morphological variability in a morphospecies exceeds its rDNA genetic variability. Such evidence for inconsistent scaling of morphological and genetic diversity in planktonic foraminifera could complicate the interpretation of evolutionary patterns in their fossil record.

Ancient Origin of the Modern Deep-Sea Fauna

The origin and possible antiquity of the spectacularly diverse modern deep-sea fauna has been debated since the beginning of deep-sea research in the mid-nineteenth century. Recent hypotheses, based on biogeographic patterns and molecular clock estimates, support a latest Mesozoic or early Cenozoic date for the origin of key groups of the present deep-sea fauna (echinoids, octopods). This relatively young age is consistent with hypotheses that argue for extensive extinction during Jurassic and Cretaceous Oceanic Anoxic Events (OAEs) and the mid-Cenozoic cooling of deep-water masses, implying repeated re-colonization by immigration of taxa from shallow-water habitats. Here we report on a well-preserved echinoderm assemblage from deep-sea (1000–1500 m paleodepth) sediments of the NE-Atlantic of Early Cretaceous age (114 Ma). The assemblage is strikingly similar to that of extant bathyal echinoderm communities in composition, including families and genera found exclusively in modern deep-sea habitats. A number of taxa found in the assemblage have no fossil record at shelf depths postdating the assemblage, which precludes the possibility of deep-sea recolonization from shallow habitats following episodic extinction at least for those groups. Our discovery provides the first key fossil evidence that a significant part of the modern deep-sea fauna is considerably older than previously assumed. As a consequence, most major paleoceanographic events had far less impact on the diversity of deep-sea faunas than has been implied. It also suggests that deep-sea biota are more resilient to extinction events than shallow-water forms, and that the unusual deep-sea environment, indeed, provides evolutionary stability which is very rarely punctuated on macroevolutionary time scales.

Vertical niche partitioning between cryptic sibling species of a cosmopolitan marine planktonic protist.

A large portion of the surface‐ocean biomass is represented by microscopic unicellular plankton. These organisms are functionally and morphologically diverse, but it remains unclear how their diversity is generated. Species of marine microplankton are widely distributed because of passive transport and lack of barriers in the ocean. How does speciation occur in a system with a seemingly unlimited dispersal potential? Recent studies using planktonic foraminifera as a model showed that even among the cryptic genetic diversity within morphological species, many genetic types are cosmopolitan, lending limited support for speciation by geographical isolation. Here we show that the current two‐dimensional view on the biogeography and potential speciation mechanisms in the microplankton may be misleading. By depth‐stratified sampling, we present evidence that sibling genetic types in a cosmopolitan species of marine microplankton, the planktonic foraminifer Hastigerina pelagica, are consistently separated by depth throughout their global range. Such strong separation between genetically closely related and morphologically inseparable genetic types indicates that niche partitioning in marine heterotrophic microplankton can be maintained in the vertical dimension on a global scale. These observations indicate that speciation along depth (depth‐parapatric speciation) can occur in vertically structured microplankton populations, facilitating diversification without the need for spatial isolation.

Phylogeography of the tropical planktonic foraminifera lineage Globigerinella reveals isolation inconsistent with passive dispersal by ocean currents

Morphologically defined species of marine plankton often harbor a considerable level of cryptic diversity. Since many morphospecies show cosmopolitan distribution, an understanding of biogeographic and evolutionary processes at the level of genetic diversity requires global sampling. We use a database of 387 single-specimen sequences of the SSU rDNA of the planktonic foraminifera Globigerinella as a model to assess the biogeographic and phylogenetic distributions of cryptic diversity in marine microplankton on a global scale. Our data confirm the existence of multiple, well isolated genetic lineages. An analysis of their abundance and distribution indicates that our sampling is likely to approximate the actual total diversity. Unexpectedly, we observe an uneven allocation of cryptic diversity among the phylogenetic lineages. We show that this pattern is neither an artifact of sampling intensity nor a function of lineage age. Instead, we argue that it reflects an ongoing speciation process in one of the three major lineages. Surprisingly, four of the six genetic types in the hyperdiverse lineage are biogeographically restricted to the Indopacific. Their mutual co-occurrence and their hierarchical phylogenetic structure provide no evidence for an origin through sudden habitat fragmentation and their limitation to the Indopacific challenges the view of a global gene flow within the warm-water provinces. This phenomenon shows that passive dispersal is not sufficient to describe the distribution of plankton diversity. Rather, these organisms show differentiated distribution patterns shaped by species interactions and reflecting phylogenetic contingency with unique histories of diversification rates.

Recent Invasion of the Symbiont-Bearing Foraminifera Pararotalia into the Eastern Mediterranean Facilitated by the Ongoing Warming Trend.

The eastern Mediterranean is a hotspot of biological invasions. Numerous species of Indo-pacific origin have colonized the Mediterranean in recent times, including tropical symbiont-bearing foraminifera. Among these is the species Pararotalia calcariformata. Unlike other invasive foraminifera, this species was discovered only two decades ago and is restricted to the eastern Mediterranean coast. Combining ecological, genetic and physiological observations, we attempt to explain the recent invasion of this species in the Mediterranean Sea. Using morphological and genetic data, we confirm the species attribution to P. calcariformata McCulloch 1977 and identify its symbionts as a consortium of diatom species dominated by Minutocellus polymorphus. We document photosynthetic activity of its endosymbionts using Pulse Amplitude Modulated Fluorometry and test the effects of elevated temperatures on growth rates of asexual offspring. The culturing of asexual offspring for 120 days shows a 30-day period of rapid growth followed by a period of slower growth. A subsequent 48-day temperature sensitivity experiment indicates a similar developmental pathway and high growth rate at 28°C, whereas an almost complete inhibition of growth was observed at 20°C and 35°C. This indicates that the offspring of this species may have lower tolerance to cold temperatures than what would be expected for species native to the Mediterranean. We expand this hypothesis by applying a Species Distribution Model (SDM) based on modern occurrences in the Mediterranean using three environmental variables: irradiance, turbidity and yearly minimum temperature. The model reproduces the observed restricted distribution and indicates that the range of the species will drastically expand westwards under future global change scenarios. We conclude that P. calcariformata established a population in the Levant because of the recent warming in the region. In line with observations from other groups of organisms, our results indicate that continued warming of the eastern Mediterranean will facilitate the invasion of more tropical marine taxa into the Mediterranean, disturbing local biodiversity and ecosystem structure.

Climate change decouples oceanic primary and export productivity and organic carbon burial

Significance Climate and ecosystem changes in the Northeast Pacific decoupled primary and export productivity and organic carbon burial during climate warming of the last deglaciation. These findings challenge and clarify the meaning of paleoceanographic proxies of productivity and provide key constraints for modeling of the ocean’s biological pump as a potential carbon feedback mechanism associated with large-scale climate change. To our knowledge, this is the first clear demonstration that primary productivity, export productivity, and carbon burial are significantly decoupled under scenarios of large-scale climate change. This is an important constraint on biogeochemical carbon cycle models, which generally assume such changes covary. Understanding responses of oceanic primary productivity, carbon export, and burial to climate change is essential for model-based projection of biological feedbacks in a high-CO2 world. Here we compare estimates of productivity based on the composition of fossil diatom floras with organic carbon burial off Oregon in the Northeast Pacific across a large climatic transition at the last glacial termination. Although estimated primary productivity was highest during the Last Glacial Maximum, carbon burial was lowest, reflecting reduced preservation linked to low sedimentation rates. A diatom size index further points to a glacial decrease (and deglacial increase) in the fraction of fixed carbon that was exported, inferred to reflect expansion, and contraction, of subpolar ecosystems that today favor smaller plankton. Thus, in contrast to models that link remineralization of carbon to temperature, in the Northeast Pacific, we find dominant ecosystem and sea floor control such that intervals of warming climate had more efficient carbon export and higher carbon burial despite falling primary productivity.

PFR2: a curated database of planktonic foraminifera 18S ribosomal DNA as a resource for studies of plankton ecology, biogeography and evolution

Planktonic foraminifera (Rhizaria) are ubiquitous marine pelagic protists producing calcareous shells with conspicuous morphology. They play an important role in the marine carbon cycle, and their exceptional fossil record serves as the basis for biochronostratigraphy and past climate reconstructions. A major worldwide sampling effort over the last two decades has resulted in the establishment of multiple large collections of cryopreserved individual planktonic foraminifera samples. Thousands of 18S rDNA partial sequences have been generated, representing all major known morphological taxa across their worldwide oceanic range. This comprehensive data coverage provides an opportunity to assess patterns of molecular ecology and evolution in a holistic way for an entire group of planktonic protists. We combined all available published and unpublished genetic data to build PFR2, the Planktonic foraminifera Ribosomal Reference database. The first version of the database includes 3322 reference 18S rDNA sequences belonging to 32 of the 47 known morphospecies of extant planktonic foraminifera, collected from 460 oceanic stations. All sequences have been rigorously taxonomically curated using a six‐rank annotation system fully resolved to the morphological species level and linked to a series of metadata. The PFR2 website, available at http://pfr2.sb-roscoff.fr, allows downloading the entire database or specific sections, as well as the identification of new planktonic foraminiferal sequences. Its novel, fully documented curation process integrates advances in morphological and molecular taxonomy. It allows for an increase in its taxonomic resolution and assures that integrity is maintained by including a complete contingency tracking of annotations and assuring that the annotations remain internally consistent.

Nanoprobe crystallographic orientation studies of isolated shield elements of the coccolithophore species Emiliania huxleyi

Coccolithophore algae produce elaborately structured skeletons composed of sub-micrometer-scale calcite crystals. In order to understand calcite crystallization and assembly in a coccosphere with nanoscale resolution, the crystal orientation and interdigitation of the structural units were investigated by transmission electron microscopy imaging, selected-area and nano-probe electron diffraction. Focused ion beam sectioning of coccoliths of the coccolithophore species Emiliania huxleyi is used to obtain target-prepared specimens in suitable orientation. We were able to detect and analyze the V-unit, which is overgrown by the R-unit. For the V-unit the 001 direction points perpendicular to the coccolith plane while the 110 axis is tangential to the coccolith ring. The R-unit c-axis is parallel and the b-axis is perpendicular to the coccolith plane, thus confirming the R- and V-model which was based on scanning electron microscopy and optical microscopy. Furthermore we show that the distal- and the proximal shield element of an individual R-unit of a single segment are tilted by 4 degrees +/- 1 degrees with respect to each other. This orientation change is required to obtain the flat domed character of the coccoliths, which is necessary to form the coccosphere. The orientation change between the distal- and the proximal shield element appears continuous.

Selective responses of benthic foraminifera to thermal pollution

Persistent thermohaline pollution at a site along the northern coast of Israel, due to power and desalination plants, is used as a natural laboratory to evaluate the effects of rising temperature and salinity levels on benthic foraminifera living in shallow hard-bottom habitats. Biomonitoring of the disturbed area and a control station shows that elevated temperature is a more significant stressor compared to salinity, thus causing a decrease in abundance and richness. Critical temperature thresholds were observed at 30 and 35°C, the latter representing the most thermally tolerant species in the studied area Pararotalia calcariformata, which is the only symbiont-bearing species observed within the core of the heated area. Common species of the shallow hard-bottom habitats including several Lessepsian invaders are almost absent in the most exposed site indicating that excess warming will likely impede the survival of these species that currently benefit from the ongoing warming of the Eastern Mediterranean.

Disruptive selection and bet-hedging in planktonic Foraminifera: shell morphology as predictor of extinctions

Extinction is a remarkably difficult phenomenon to study under natural conditions. This is because the outcome of stress exposure and associated fitness reduction is not known until the extinction occurs and it remains unclear whether there is any phenotypic reaction of the exposed population that can be used to predict its fate. Here we take advantage of the fossil record, where the ecological outcome of stress exposure is known. Specifically, we analyze shell morphology of planktonic Foraminifera in sediment samples from the Mediterranean, during an interval preceding local extinctions. In two species representing different plankton habitats, we observe shifts in trait state and decrease in variance in association with non-terminal stress, indicating stabilizing selection. At terminal stress levels, immediately before extinction, we observe increased growth asymmetry and trait variance, indicating disruptive selection and bet-hedging. The pre-extinction populations of both species show a combination of trait states and trait variance distinct from all populations exposed to non-terminal levels of stress. This finding indicates that the phenotypic history of a population may allow the detection of threshold levels of stress, likely to lead to extinction. It is thus an alternative to population dynamics in studying and monitoring natural population ecology.