Evolutionary Turnover Research Articles

Sex determination, longevity, and the birth and death of reptilian species.

Vertebrate sex‐determining mechanisms (SDMs) are triggered by the genotype (GSD), by temperature (TSD), or occasionally, by both. The causes and consequences of SDM diversity remain enigmatic. Theory predicts SDM effects on species diversification, and life‐span effects on SDM evolutionary turnover. Yet, evidence is conflicting in clades with labile SDMs, such as reptiles. Here, we investigate whether SDM is associated with diversification in turtles and lizards, and whether alterative factors, such as lifespan's effect on transition rates, could explain the relative prevalence of SDMs in turtles and lizards (including and excluding snakes). We assembled a comprehensive dataset of SDM states for squamates and turtles and leveraged large phylogenies for these two groups. We found no evidence that SDMs affect turtle, squamate, or lizard diversification. However, SDM transition rates differ between groups. In lizards TSD‐to‐GSD surpass GSD‐to‐TSD transitions, explaining the predominance of GSD lizards in nature. SDM transitions are fewer in turtles and the rates are similar to each other (TSD‐to‐GSD equals GSD‐to‐TSD), which, coupled with TSD ancestry, could explain TSD's predominance in turtles. These contrasting patterns can be explained by differences in life history. Namely, our data support the notion that in general, shorter lizard lifespan renders TSD detrimental favoring GSD evolution in squamates, whereas turtle longevity permits TSD retention. Thus, based on the macro‐evolutionary evidence we uncovered, we hypothesize that turtles and lizards followed different evolutionary trajectories with respect to SDM, likely mediated by differences in lifespan. Combined, our findings revealed a complex evolutionary interplay between SDMs and life histories that warrants further research that should make use of expanded datasets on unexamined taxa to enable more conclusive analyses.

Stirring the Melting Pot

Stirring the Melting Pot

Dynamics of abundance of the mid- to late Pridoli conodonts from the eastern part of the Silurian Baltic basin: Multifractals, state shifts, and oscillations

The Pridoli epoch is one of the most geobiologically unstable intervals in the Silurian period. However, the ecological and evolutionary dynamics of the biota from this time are still poorly understood. Here we present a comprehensive quantitative time-series analyses of conodont abundances during the middle and the upper parts of the Pridoli epoch. The study reveals that the stratigraphic series of conodont abundances has a multifractal structure. This feature implies the presence of multiple serially correlated processes hierarchically operating on different time scales and interacting in a multiplicative fashion. Estimation of a maximal Lyapunov exponent and a test for presence of determinism also revealed a chaotic and non-linear low-dimensional nature of long-term conodont abundance dynamics. The most probable (but not exclusive) mechanism for the origin of chaos in the time series of conodont abundance is that conodont abundances tracked changes in crucial environmental parameters, most probably related to the climate that exhibits long term chaos. The complex and non-linear nature of the conodont dynamics is also revealed by a moving-window correlation analyses of conodont abundances and by an environmental proxy time series. We found three alternating episodes of different correlation patterns between conodont abundances and the δ13C record. In the middle and upper most Pridoli interval there are positive but statistically non-significant correlations between these two variables. In contrast the lower part of the upper Pridoli (middle of the Jūra formation) exhibits negative and statistically significant correlation between the variables. In addition moving-window standard deviation analyses reveals that during the transitions between these episodes, there were abrupt changes in the variance in both the carbon isotopes and the conodont abundances, which implies that these episodes represent alternative states in the way the earth system functioned that were punctuated by the critical transitions between them. The interval with negative correlations between abundances and isotopes was also marked by a profound evolutionary turnover of acanthodians and to lesser extent conodonts. This interval most probably represented an anomalous time, with differing ecological rules and increased macroevolutionary rates, which can be interpreted as a turnover pulse. The spectral cyclostratigraphic analyses of the abundance data reveals that conodont abundances also exhibited periodic oscillations at several frequencies. The cycles determined for the analysis have the period lengths of 56, 99, 127 and 950 Ka, which probably were caused by the periodic changes in the obliquity and eccentricity of Earth9s orbit. The proposed proximate mechanism that controlled cyclic changes in the abundances of conodonts, based on the climatological deductions, was a variation in nutrients supplies that was due to changes in the degree of seasonality in the tropics, driven by Milankovitch cycles. It is probable that the described state shifts in the way that the ecosystem functioned were also forced by long-term Milankovitch cycles.

Evolutionary Turnover of Kinetochore Proteins: A Ship of Theseus?

The kinetochore is a multiprotein complex that mediates the attachment of a eukaryotic chromosome to the mitotic spindle. The protein composition of kinetochores is similar across species as divergent as yeast and human. However, recent findings have revealed an unexpected degree of compositional diversity in kinetochores. For example, kinetochore proteins that are essential in some species have been lost in others, whereas new kinetochore proteins have emerged in other lineages. Even in lineages with similar kinetochore composition, individual kinetochore proteins have functionally diverged to acquire either essential or redundant roles. Thus, despite functional conservation, the repertoire of kinetochore proteins has undergone recurrent evolutionary turnover.

Duplication and Diversification of Dipteran Argonaute Genes, and the Evolutionary Divergence of Piwi and Aubergine.

Genetic studies of Drosophila melanogaster have provided a paradigm for RNA interference (RNAi) in arthropods, in which the microRNA and antiviral pathways are each mediated by a single Argonaute (Ago1 and Ago2) and germline suppression of transposable elements is mediated by a trio of Piwi-subfamily Argonaute proteins (Ago3, Aub, and Piwi). Without a suitable evolutionary context, deviations from this can be interpreted as derived or idiosyncratic. Here we analyze the evolution of Argonaute genes across the genomes and transcriptomes of 86 Dipteran species, showing that variation in copy number can occur rapidly, and that there is constant flux in some RNAi mechanisms. The lability of the RNAi pathways is illustrated by the divergence of Aub and Piwi (182–156 Ma), independent origins of multiple Piwi-family genes in Aedes mosquitoes (less than 25Ma), and the recent duplications of Ago2 and Ago3 in the tsetse fly Glossina morsitans. In each case the tissue specificity of these genes has altered, suggesting functional divergence or innovation, and consistent with the action of dynamic selection pressures across the Argonaute gene family. We find there are large differences in evolutionary rates and gene turnover between pathways, and that paralogs of Ago2, Ago3, and Piwi/Aub show contrasting rates of evolution after duplication. This suggests that Argonautes undergo frequent evolutionary expansions that facilitate functional divergence.

The evolutionary turnover of recombination hot spots contributes to speciation in mice.

Meiotic recombination is required for the segregation of homologous chromosomes and is essential for fertility. In most mammals, the DNA double-strand breaks (DSBs) that initiate meiotic recombination are directed to a subset of genomic loci (hot spots) by sequence-specific binding of the PRDM9 protein. Rapid evolution of the DNA-binding specificity of PRDM9 and gradual erosion of PRDM9-binding sites by gene conversion will alter the recombination landscape over time. To better understand the evolutionary turnover of recombination hot spots and its consequences, we mapped DSB hot spots in four major subspecies of Mus musculus with different Prdm9 alleles and in their F1 hybrids. We found that hot spot erosion governs the preferential usage of some Prdm9 alleles over others in hybrid mice and increases sequence diversity specifically at hot spots that become active in the hybrids. As crossovers are disfavored at such hot spots, we propose that sequence divergence generated by hot spot turnover may create an impediment for recombination in hybrids, potentially leading to reduced fertility and, eventually, speciation.

Greenhouse−icehouse transition in the Late Ordovician marks a step change in extinction regime in the marine plankton

Two distinct regimes of extinction dynamic are present in the major marine zooplankton group, the graptolites, during the Ordovician and Silurian periods (486-418 Ma). In conditions of "background" extinction, which dominated in the Ordovician, taxonomic evolutionary rates were relatively low and the probability of extinction was highest among newly evolved species ("background extinction mode"). A sharp change in extinction regime in the Late Ordovician marked the onset of repeated severe spikes in the extinction rate curve; evolutionary turnover increased greatly in the Silurian, and the extinction mode changed to include extinction that was independent of species age ("high-extinction mode"). This change coincides with a change in global climate, from greenhouse to icehouse conditions. During the most extreme episode of extinction, the Late Ordovician Mass Extinction, old species were selectively removed ("mass extinction mode"). Our analysis indicates that selective regimes in the Paleozoic ocean plankton switched rapidly (generally in <0.5 My) from one mode to another in response to environmental change, even when restoration of the full ecosystem was much slower (several million years). The patterns observed are not a simple consequence of geographic range effects or of taxonomic changes from Ordovician to Silurian. Our results suggest that the dominant primary controls on extinction throughout the lifespan of this clade were abiotic (environmental), probably mediated by the microphytoplankton.

The Origins of Tropical Rainforest Hyperdiversity.

Traditional models for tropical species richness contrast rainforests as "museums" of old species or "cradles" of recent speciation. High plant species diversity in rainforests may be more likely to reflect high episodic evolutionary turnover of species--a scenario implicating high rates of both speciation and extinction through geological time.

High evolutionary turnover of satellite families in Caenorhabditis.

BackgroundThe high density of tandem repeat sequences (satellites) in nematode genomes and the availability of genome sequences from several species in the group offer a unique opportunity to better understand the evolutionary dynamics and the functional role of these sequences. We take advantage of the previously developed SATFIND program to study the satellites in four Caenorhabditis species and investigate these questions.MethodsThe identification and comparison of satellites is carried out in three steps. First we find all the satellites present in each species with the SATFIND program. Each satellite is defined by its length, number of repeats, and repeat sequence. Only satellites with at least ten repeats are considered. In the second step we build satellite families with a newly developed alignment program. Satellite families are defined by a consensus sequence and the number of satellites in the family. Finally we compare the consensus sequence of satellite families in different species.ResultsWe give a catalog of individual satellites in each species. We have also identified satellite families with a related sequence and compare them in different species. We analyze the turnover of satellites: they increased in size through duplications of fragments of 100-300 bases. It appears that in many cases they have undergone an explosive expansion. In C. elegans we have identified a subset of large satellites that have strong affinity for the centromere protein CENP-A. We have also compared our results with those obtained from other species, including one nematode and three mammals.ConclusionsMost satellite families found in Caenorhabditis are species-specific; in particular those with long repeats. A subset of these satellites may facilitate the formation of kinetochores in mitosis. Other satellite families in C. elegans are either related to Helitron transposons or to meiotic pairing centers.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0495-x) contains supplementary material, which is available to authorized users.

Evolution of DNA-Binding Sites of a Floral Master Regulatory Transcription Factor.

Flower development is controlled by the action of key regulatory transcription factors of the MADS-domain family. The function of these factors appears to be highly conserved among species based on mutant phenotypes. However, the conservation of their downstream processes is much less well understood, mostly because the evolutionary turnover and variation of their DNA-binding sites (BSs) among plant species have not yet been experimentally determined. Here, we performed comparative ChIP (chromatin immunoprecipitation)-seq experiments of the MADS-domain transcription factor SEPALLATA3 (SEP3) in two closely related Arabidopsis species: Arabidopsis thaliana and A. lyrata which have very similar floral organ morphology. We found that BS conservation is associated with DNA sequence conservation, the presence of the CArG-box BS motif and on the relative position of the BS to its potential target gene. Differences in genome size and structure can explain that SEP3 BSs in A. lyrata can be located more distantly to their potential target genes than their counterparts in A. thaliana. In A. lyrata, we identified transposition as a mechanism to generate novel SEP3 binding locations in the genome. Comparative gene expression analysis shows that the loss/gain of BSs is associated with a change in gene expression. In summary, this study investigates the evolutionary dynamics of DNA BSs of a floral key-regulatory transcription factor and explores factors affecting this phenomenon.

A new Permian bivalve-dominated assemblage in the Rio do Rasto Formation, Paraná Basin, Brazil: Faunal turnover driven by regional-scale environmental changes in a vast epeiric sea

The basal portion of the Permian Rio do Rasto Formation (Serrinha Member), Passa Dois Group, Paraná Basin, Brazil, records an entirely new bivalve fauna intercalated between the underlying Pinzonella neotropica assemblage (uppermost portion of the Teresina Formation) and the overlying Leinzia similis assemblage (Rio do Rasto Formation). Mollusks of these assemblages lived in marginal shallow-water habitats of an immense epeiric sea and were dominated by endemic bivalve species. Taxonomic analysis revealed the presence of Terraia curvata (60.61%), Astartellopsis prosoclina (19.70%), Cowperesia emerita (10.61%), Leinzia curta (4.55%), Terraia bipleura (3.03%) and Beurlenella elongatella (1.52%), which are associated with conchostracans and plant remains. Species composition, abundance, and dominance in this novel assemblage differ notably from the preceding ones, suggesting a substantial evolutionary turnover. Regional-scale environmental changes recognized based on taphonomy, facies analysis, and geochemical data consist of progressive freshening of the marginal habitats of the Paraná Basin and taxic changes that include the following: (a) loss of genera, (b) decrease in bivalve abundance and ecological guilds, (c) disappearance of the dominant bivalve group (Pinzonellinae) and (d) diversification of Terrainae bivalves. The ecological signature also changed notably because only infaunal suspension-feeding bivalves are present, indicating a significant loss of functional diversity at the regional scale. Likely stressor factors (among others) are tied to freshening events, suggesting profound changes in (a) salinity, (b) primary productivity and (c) a lack of coarse, stable substrates coupled with high bioturbation rates. Hence, our regional example could offer valuable clues to benthic (bivalve) community responses in a habitat subjected to (a) rapid climate changes and (b) freshening events in shallow-water settings. Finally, the stratigraphic range of the dominant species (T. curvata) appears to be restricted to the basal portion of the Rio do Rasto Formation. Based on the presence of this species and of C. emerita, the novel assemblage is tentatively correlated with that of the Permian Gai-As Formation in the Huab region of Namibia, thus supporting previous assumptions of a seaway connecting both basins during the Guadalupian Epoch.

Continuous evolutionary change in Plio-Pleistocene mammals of eastern Africa

Much debate has revolved around the question of whether the mode of evolutionary and ecological turnover in the fossil record of African mammals was continuous or pulsed, and the degree to which faunal turnover tracked changes in global climate. Here, we assembled and analyzed large specimen databases of the fossil record of eastern African Bovidae (antelopes) and Turkana Basin large mammals. Our results indicate that speciation and extinction proceeded continuously throughout the Pliocene and Pleistocene, as did increases in the relative abundance of arid-adapted bovids, and in bovid body mass. Species durations were similar among clades with different ecological attributes. Occupancy patterns were unimodal, with long and nearly symmetrical origination and extinction phases. A single origination pulse may be present at 2.0-1.75 Ma, but besides this, there is no evidence that evolutionary or ecological changes in the eastern African record tracked rapid, 100,000-y-scale changes in global climate. Rather, eastern African large mammal evolution tracked global or regional climatic trends at long (million year) time scales, while local, basin-scale changes (e.g., tectonic or hydrographic) and biotic interactions ruled at shorter timescales.

Transcriptome Differences between Alternative Sex Determining Genotypes in the House Fly, Musca domestica.

Sex determination evolves rapidly, often because of turnover of the genes at the top of the pathway. The house fly, Musca domestica, has a multifactorial sex determination system, allowing us to identify the selective forces responsible for the evolutionary turnover of sex determination in action. There is a male determining factor, M, on the Y chromosome (YM), which is probably the ancestral state. An M factor on the third chromosome (IIIM) has reached high frequencies in multiple populations across the world, but the evolutionary forces responsible for the invasion of IIIM are not resolved. To test whether the IIIM chromosome invaded because of sex-specific selection pressures, we used mRNA sequencing to determine whether isogenic males that differ only in the presence of the YM or IIIM chromosome have different gene expression profiles. We find that more genes are differentially expressed between YM and IIIM males in testis than head, and that genes with male-biased expression are most likely to be differentially expressed between YM and IIIM males. We additionally find that IIIM males have a “masculinized” gene expression profile, suggesting that the IIIM chromosome has accumulated an excess of male-beneficial alleles because of its male-limited transmission. These results are consistent with the hypothesis that sex-specific selection acts on alleles linked to the male-determining locus driving evolutionary turnover in the sex determination pathway.

Lessons from modENCODE.

The modENCODE (Model Organism Encyclopedia of DNA Elements) Consortium aimed to map functional elements-including transcripts, chromatin marks, regulatory factor binding sites, and origins of DNA replication-in the model organisms Drosophila melanogaster and Caenorhabditis elegans. During its five-year span, the consortium conducted more than 2,000 genome-wide assays in developmentally staged animals, dissected tissues, and homogeneous cell lines. Analysis of these data sets provided foundational insights into genome, epigenome, and transcriptome structure and the evolutionary turnover of regulatory pathways. These studies facilitated a comparative analysis with similar data types produced by the ENCODE Consortium for human cells. Genome organization differs drastically in these distant species, and yet quantitative relationships among chromatin state, transcription, and cotranscriptional RNA processing are deeply conserved. Of the many biological discoveries of the modENCODE Consortium, we highlight insights that emerged from integrative studies. We focus on operational and scientific lessons that may aid future projects of similar scale or aims in other, emerging model systems.

Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations.

ABSTRACTAlthough plasmids and other episomes are recognized as key players in horizontal gene transfer among microbes, their diversity and dynamics among ecologically structured host populations in the wild remain poorly understood. Here, we show that natural populations of marine Vibrionaceae bacteria host large numbers of families of episomes, consisting of plasmids and a surprisingly high fraction of plasmid-like temperate phages. Episomes are unevenly distributed among host populations, and contrary to the notion that high-density communities in biofilms act as hot spots of gene transfer, we identified a strong bias for episomes to occur in free-living as opposed to particle-attached cells. Mapping of episomal families onto host phylogeny shows that, with the exception of all phage and a few plasmid families, most are of recent evolutionary origin and appear to have spread rapidly by horizontal transfer. Such high eco-evolutionary turnover is particularly surprising for plasmids that are, based on previously suggested categorization, putatively nontransmissible, indicating that this type of plasmid is indeed frequently transferred by currently unknown mechanisms. Finally, analysis of recent gene transfer among plasmids reveals a network of extensive exchange connecting nearly all episomes. Genes functioning in plasmid transfer and maintenance are frequently exchanged, suggesting that plasmids can be rapidly transformed from one category to another. The broad distribution of episomes among distantly related hosts and the observed promiscuous recombination patterns show how episomes can offer their hosts rapid assembly and dissemination of novel functions.

Origin, evolution, and population genetics of the selfish Segregation Distorter gene duplication in European and African populations of Drosophila melanogaster.

Meiotic drive elements are a special class of evolutionarily "selfish genes" that subvert Mendelian segregation to gain preferential transmission at the expense of homologous loci. Many drive elements appear to be maintained in populations as stable polymorphisms, their equilibrium frequencies determined by the balance between drive (increasing frequency) and selection (decreasing frequency). Here we show that a classic, seemingly balanced, drive system is instead characterized by frequent evolutionary turnover giving rise to dynamic, rather than stable, equilibrium frequencies. The autosomal Segregation Distorter (SD) system of the fruit fly Drosophila melanogaster is a selfish coadapted meiotic drive gene complex in which the major driver corresponds to a partial duplication of the gene Ran-GTPase activating protein (RanGAP). SD chromosomes segregate at similar, low frequencies of 1-5% in natural populations worldwide, consistent with a balanced polymorphism. Surprisingly, our population genetic analyses reveal evidence for parallel, independent selective sweeps of different SD chromosomes in populations on different continents. These findings suggest that, rather than persisting at a single stable equilibrium, SD chromosomes turn over frequently within populations.

An engine for global plant diversity: highest evolutionary turnover and emigration in the American tropics.

Understanding the processes that have generated the latitudinal biodiversity gradient and the continental differences in tropical biodiversity remains a major goal of evolutionary biology. Here we estimate the timing and direction of range shifts of extant flowering plants (angiosperms) between tropical and non-tropical zones, and into and out of the major tropical regions of the world. We then calculate rates of speciation and extinction taking into account incomplete taxonomic sampling. We use a recently published fossil calibrated phylogeny and apply novel bioinformatic tools to code species into user-defined polygons. We reconstruct biogeographic history using stochastic character mapping to compute relative numbers of range shifts in proportion to the number of available lineages through time. Our results, based on the analysis of c. 22,600 species and c. 20 million geo-referenced occurrence records, show no significant differences between the speciation and extinction of tropical and non-tropical angiosperms. This suggests that at least in plants, the latitudinal biodiversity gradient primarily derives from other factors than differential rates of diversification. In contrast, the outstanding species richness found today in the American tropics (the Neotropics), as compared to tropical Africa and tropical Asia, is associated with significantly higher speciation and extinction rates. This suggests an exceedingly rapid evolutionary turnover, i.e., Neotropical species being formed and replaced by one another at unparalleled rates. In addition, tropical America stands out from other continents by having “pumped out” more species than it received through most of the last 66 million years. These results imply that the Neotropics have acted as an engine for global plant diversity.

A method for calculating probabilities of fitness consequences for point mutations across the human genome.

We describe a novel computational method for estimating the probability that a point mutation at each position in a genome will influence fitness. These fitness consequence (fitCons) scores serve as evolution-based measures of potential genomic function. Our approach is to cluster genomic positions into groups exhibiting distinct “fingerprints” based on high-throughput functional genomic data, then to estimate a probability of fitness consequences for each group from associated patterns of genetic polymorphism and divergence. We have generated fitCons scores for three human cell types based on public data from ENCODE. Compared with conventional conservation scores, fitCons scores show considerably improved prediction power for cis-regulatory elements. In addition, fitCons scores indicate that 4.2–7.5% of nucleotides in the human genome have influenced fitness since the human-chimpanzee divergence, and they suggest that recent evolutionary turnover has had limited impact on the functional content of the genome.

Altered chromatin occupancy of master regulators underlies evolutionary divergence in the transcriptional landscape of erythroid differentiation.

Erythropoiesis is one of the best understood examples of cellular differentiation. Morphologically, erythroid differentiation proceeds in a nearly identical fashion between humans and mice, but recent evidence has shown that networks of gene expression governing this process are divergent between species. We undertook a systematic comparative analysis of six histone modifications and four transcriptional master regulators in primary proerythroblasts and erythroid cell lines to better understand the underlying basis of these transcriptional differences. Our analyses suggest that while chromatin structure across orthologous promoters is strongly conserved, subtle differences are associated with transcriptional divergence between species. Many transcription factor (TF) occupancy sites were poorly conserved across species (∼25% for GATA1, TAL1, and NFE2) but were more conserved between proerythroblasts and cell lines derived from the same species. We found that certain cis-regulatory modules co-occupied by GATA1, TAL1, and KLF1 are under strict evolutionary constraint and localize to genes necessary for erythroid cell identity. More generally, we show that conserved TF occupancy sites are indicative of active regulatory regions and strong gene expression that is sustained during maturation. Our results suggest that evolutionary turnover of TF binding sites associates with changes in the underlying chromatin structure, driving transcriptional divergence. We provide examples of how this framework can be applied to understand epigenomic variation in specific regulatory regions, such as the β-globin gene locus. Our findings have important implications for understanding epigenomic changes that mediate variation in cellular differentiation across species, while also providing a valuable resource for studies of hematopoiesis.

Biometry of Upper Cretaceous (Cenomanian–Maastrichtian) coccoliths – a record of long-term stability and interspecies size shifts

Biometric measurements of Mesozoic coccoliths (coccolith length and width) have been used in short-term biostratigraphic, taxonomic and palaeoecologic studies, but until now, not over longer time scales. Here, we present a long time-series study (∼30million years) for the Upper Cretaceous, which aims to identify broad trends in coccolith size and to understand the factors governing coccolith size change over long time scales. We have generated biometric data for the dominant Upper Cretaceous coccolith groups, Broinsonia/Arkhangelskiella, Prediscosphaera, Retecapsa and Watznaueria, from 36 Cenomanian–Maastrichtian (100.5–66Ma) samples from Goban Spur in the northeast Atlantic (DSDP Site 549). These data show that the coccolith sizes within Prediscosphaera, Retecapsa and Watznaueria were relatively stable through the Late Cretaceous, with mean size variation less than 0.7μm. Within the Broinsonia/Arkhangelskiella group there was more pronounced variation, with a mean size increase from∼6μm in the Cenomanian to∼10μm in the Campanian. This significant change in mean size was largely driven by evolutionary turnover (species origination and extinctions), and, in particular, the appearance of larger species/subspecies (Broinsonia parca parca, Broinsonia parca constricta, Arkhangelskiella cymbiformis) in the early Campanian, replacing smaller species, such as Broinsonia signata and Broinsonia enormis. Shorter-term size fluctuations within Broinsonia/Arkhangelskiella, observed across the Late Cenomanian–Turonian and Late Campanian–Maastrichtian intervals, may, however, reflect changing palaeoenvironmental conditions, such as sea surface temperature and nutrient availability.