Integral projection model results of the planktonic foraminifer Trilobatus sacculifer

R is required to open the Supplementary Code,Developmental plasticity, where traits change state in response to environmental cues, is well-studied in modern populations. It is also suspected to play a role in macroevolutionary dynamics, but due to a lack of long-term records the frequency of plasticity-led evolution in deep time remains unknown. Populations are dynamic entities, yet their representation in the fossil record is a static snapshot of often isolated individuals. Here, we apply for the first time contemporary integral projection models (IPMs) to fossil data to link individual development with expected population variation. IPMs describe the effects of individual growth in discrete steps on long-term population dynamics. We parameterize the models using modern and fossil data of the planktonic foraminifer Trilobatus sacculifer. Foraminifera grow by adding chambers in discrete stages and die at reproduction, making them excellent case studies for IPMs. Our results predict that somatic growth rates have almost twice as much influence on population dynamics than survival and more than eight times more influence than reproduction, suggesting that selection would primarily target somatic growth as the major determinant of fitness. As numerous palaeobiological systems record growth rate increments in single genetic individuals, and imaging technologies are increasingly available, our results open up the possibility of evidence-based inference of developmental plasticity spanning macroevolutionary dynamics. Given the centrality of ecology in palaeobiological thinking, our model is one approach to help bridge eco-evolutionary scales while directing attention towards the most relevant life-history traits to measure.</span

Developmental plasticity in deep time: a window to population ecological inference

Developmental plasticity, where traits change state in response to environmental cues, is well-studied in modern populations. It is also suspected to play a role in macroevolutionary dynamics, but due to a lack of long-term records the frequency of plasticity-led evolution in deep time remains unknown. Populations are dynamic entities, yet their representation in the fossil record is a static snapshot of often isolated individuals. Here, we apply for the first time contemporary integral projection models (IPMs) to fossil data to link individual development with expected population variation. IPMs describe the effects of individual growth in discrete steps on long-term population dynamics. We parameterize the models using modern and fossil data of the planktonic foraminifer Trilobatus sacculifer. Foraminifera grow by adding chambers in discrete stages and die at reproduction, making them excellent case studies for IPMs. Our results predict that somatic growth rates have almost twice as much influence on population dynamics than survival and more than eight times more influence than reproduction, suggesting that selection would primarily target somatic growth as the major determinant of fitness. As numerous palaeobiological systems record growth rate increments in single genetic individuals, and imaging technologies are increasingly available, our results open up the possibility of evidence-based inference of developmental plasticity spanning macroevolutionary dynamics. Given the centrality of ecology in palaeobiological thinking, our model is one approach to help bridge eco-evolutionary scales while directing attention towards the most relevant life-history traits to measure

Calibration of the repeatability of foraminiferal test size and shape measures with recommendations for future use

The fossil record of planktonic foraminifera is ideally suited to defining stratigraphic age controls and exploring fundamental questions in evolutionary biology due to its excellent preservation potential that yields continuous, high-resolution fossil archives of large numbers of individuals. For full morphometric analyses foraminifera tests are generally mounted, oriented and imaged manually, while data are processed using standard software such as ImageJ or Image Pro. However, manually induced orientation errors are a source of potential bias in trait measurements even when quantified using the same computational subroutine. Here we test the repeatability of four measures of foraminiferal test shape on six morphologically distinct species and present a calibration (power analysis) of the number of individuals needed to determine a given percentage change in these traits. We mounted and measured every individual twice and analysed the difference between the two measurements to determine the effects of small orientation changes on the studied traits. We show that measurements of test area and aspect ratio are statistically indistinguishable between runs for all species studied, and a power law calibration suggests that between 25 and 50 individuals are needed to detect at least a 10% in- or decrease in either trait. However, despite mounting tests on glass slides to clarify perimeter outlines, test perimeter was only repeatable in the spherical species Orbulina universa, and test roundness was not repeatable for three out of six studied species. We recommend the use of lengths and avoidance of perimeters and their dependent metrics to reduce orientation induced bias

The dynamics of diachronous extinction associated with climatic deterioration near the neogene/quaternary boundary

To predict extinction we must understand the processes leading to population decline. Once a critical threshold of population size is reached, small environmental perturbations can push a species over the cliff-edge to extinction, so the main drivers of extinction are the factors that cause the initial reduction in population size. Most studies of population decline leading up to extinction focus on modern species, the extinction of which is often dominantly driven by humans. The drivers of population decline leading to non-human mediated extinctions are less well known but changes in climate are arguably the most widely invoked mechanism. Here, we report data on &gt;16,000 individuals of the planktonic foraminifer Globoconella puncticulata from six sites in the Atlantic Ocean along a 83 degree-long latitudinal transect, over a 600,000-year interval leading up to the species’ global extinction during the late Pliocene-earliest Pleistocene intensification of Northern Hemisphere glaciation. We show changes in geographic range, abundance and body size. We find that populations do not follow a North-to-South sequence in extinction as Earth cooled and developed large ice sheets in the high latitudes of the Northern Hemisphere. Instead, our results suggest that populations are differentially adapted to local environmental settings, that population dynamics in core populations differ from those at the edge of their range, and that individual population responses to external pressures are essential to understanding the drivers of global extinction. Our study demonstrates the potential to transform our understanding of extinction dynamics through spatially replicated sampling of the highly-resolved marine microfossil record

Size and shape data of Globigerinoidesella fistulosa, Trilobatus sacculifer and intermediate specimens from ODP Site 1115

Planktonic foraminifera are extremely well-suited to study evolutionary processes in the fossil record due to their high-resolution deposits and global distribution. Species are typically conservative in their shell morphology with the same geometric shapes appearing repeatedly through iterative evolution, but the mechanisms behind the architectural limits on foraminiferal shell shape are still not well understood. To understand when and how these developmental constraints can be overcome, we study morphological change leading up to the origination of the unusually ornate species Globigerinoidesella fistulosa. Our results show that the origination of G. fistulosa from the Trilobatus sacculifer plexus involved an amalgamation of three different heterochronic expressions: addition of chambers (hypermorphosis), earlier onset of protuberances (pre-displacement), and steeper allometric slope (acceleration) as compared to its ancestor. We argue that the protuberances unique to G. fistulosa were necessary to sustain a surface-area: volume ratio that could host sufficient numbers of photosymbionts. Our work provides a case study of the complex combination of processes required to produce unusual shell shapes and highlights the importance of developmental processes in evolutionary origination.</span

Analysing planktonic foraminiferal growth in three dimensions with foram3D: an R package for automated trait measurements from CT scans

Foraminifera are one of the few taxa that preserve their entire ontogeny in their fossilised remains. Revealing this ontogeny through micro-computed tomography (CT) of fossil planktonic foraminifera has greatly improved our understanding of their life history and allows accurate quantification of total shell volume, growth rates and developmental constraints throughout an individual's life. Studies using CT scans currently mainly focus on chamber size, but the wealth of three-dimensional data generated by CT scans has the potential to reconstruct complete growth trajectories. Here we present an open-source R package to analyse growth in three-dimensional space. Using only the centroid xyz coordinates of every chamber, the functions determine the growth sequence and check that chambers are in the correct order. Once the order of growth has been verified, the functions calculate distances and angles between subsequent chambers, determine the total number of whorls and the number of chambers in the final whorl at the time each chamber was built, and, for the first time, quantify trochospirality. The applications of this package will enable repeatable analysis of large data sets and quantification of key taxonomic traits and ultimately provide new insights into the effects of ontogeny on evolution

The breakdown of static and evolutionary allometries during climatic upheaval

The influence of within-species variation and covariation on evolutionary patterns is well established for generational and macroevolutionary processes, most prominently through genetic lines of least resistance. However, it is not known whether intraspecific phenotypic variation also directs microevolutionary trajectories into the long term when a species is subject to varying environmental conditions. Here we present a continuous, high-resolution bivariate record of size and shape changes among 12,633 individual planktonic foraminifera of a surviving and an extinct-going species over 500 thousand years. This time interval spans the late Pliocene to earliest Pleistocene intensification of Northern Hemisphere glaciation, an interval of profound climate upheaval that can be divided into three phases of increasing glacial intensity. We found that within each of these three Plio-Pleistocene climate phases the within-population allometries predict evolutionary change from one time-step to the next, and that the within-phase among-population (i.e. evolutionary) allometries match their corresponding static (within-population) allometries. However, the evolutionary allometry across the three climate phases deviates significantly from the static and phase-specific evolutionary allometries in the extinct-going species. Although intraspecific variation leaves a clear signature on mean evolutionary change from one time-step to the next, our study suggests that the link between intraspecific variation and longer-term micro- and macroevolutionary phenomena is prone to environmental perturbation that can overcome constraints induced by within-species trait covariation

Shall area and aspect ratio of G. puncticulata and T. crassaformis

Shell size and shape of the planktonic foraminifera species Globoconella puncticulata and Truncorotalia crassaformis are presented, with sample ID. Sample age as determined by the age model by Bolton et al., 2010 (Paleoceanography)

Heterochrony in the evolution of the planktonic foraminifer Globigerinoidesella fistulosa from the <i>Trilobatus sacculifer</i> plexus

Planktonic foraminifera are extremely well-suited to study evolutionary change in the fossil record due to their high-resolution deposits and global distribution. Species are typically conservative in their shell morphology with the same geometric shapes appearing repeatedly through iterative evolution, but the mechanisms behind the architectural limits on foraminiferal shell shape are still not well understood. To understand when and how these developmental constraints evolve, we study morphological change leading up to the origination of the unusually ornate species Globigerinoidesella fistulosa. We measured the size and circularity of over 900 specimens of G. fistulosa, its ancestor Trilobatus sacculifer and intermediate forms from a site in the Western Equatorial Pacific. Our results show that the origination of G. fistulosa from the Trilobatus sacculifer plexus involved a combination of two heterochronic expressions: earlier onset of protuberances (pre-displacement) and steeper allometric slope (acceleration) as compared to its ancestor. Our work provides a case study of the complex morphological and developmental changes required to produce unusual shell shapes and highlights the importance of developmental changes in evolutionary origination