A 15-million-year-long record of phenotypic evolution in the heavily calcified coccolithophore <i>Helicosphaera</i> and its biogeochemical implications

Abstract

Abstract. The biogeochemical impact of coccolithophores is defined not only by their overall abundance in the oceans but also by wide ranges in physiological traits such as cell size, degree of calcification and carbon production rates between different species. Species' sensitivity to environmental forcing has been suggested to relate to their cellular PIC : POC (particulate inorganic carbon : particulate organic carbon) ratio and other physiological constraints. Understanding both the short-term and longer-term adaptive strategies of different coccolithophore lineages, and how these in turn shape the biogeochemical role of the group, is therefore crucial for modeling the ongoing changes in the global carbon cycle. Here we present data on the phenotypic evolution of a large and heavily calcified genus Helicosphaera (order Zygodiscales) over the past 15 million years (Myr), at two deep-sea drill sites in the tropical Indian Ocean and temperate South Atlantic. The modern species Helicosphaera carteri, which displays ecophysiological adaptations in modern strains, was used to benchmark the use of its coccolith morphology as a physiological proxy in the fossil record. Our results show that, on the single-genotype level, coccolith morphology has no correlation with growth rates, cell size or PIC and POC production rates in H. carteri. However, significant correlations of coccolith morphometric parameters with cell size and physiological rates do emerge once multiple genotypes or closely related lineages are pooled together. Using this insight, we interpret the phenotypic evolution in Helicosphaera as a global, resource-limitation-driven selection for smaller cells, which appears to be a common adaptive trait among different coccolithophore lineages, from the warm and high-CO2 world of the middle Miocene to the cooler and low-CO2 conditions of the Pleistocene. However, despite a significant decrease in mean coccolith size and cell size, Helicosphaera kept a relatively stable PIC : POC ratio (as inferred from the coccolith aspect ratio) and thus highly conservative biogeochemical output on the cellular level. We argue that this supports its status as an obligate calcifier, like other large and heavily calcified genera such as Calcidiscus and Coccolithus, and that other adaptive strategies, beyond size adaptation, must support the persistent, albeit less abundant, occurrence of these taxa. This is in stark contrast with the ancestral lineage of Emiliania and Gephyrocapsa, which not only decreased in mean size but also displayed much higher phenotypic plasticity in their degree of calcification while becoming globally more dominant in plankton communities.

Evolutionary Rates in the Haptophyta: Exploring Molecular and Phenotypic Diversity

“…Indeed, the selection for smaller morphotypes appears to be a common long-term adaptive response across multiple coccolithophore lineages over the past 15 million years. Detailed biometric time series data of several key taxa support that this selection for smaller cells occurred across various scales: (a) the (morpho)species level, (b) the community level, as well as (c) the evolutionary level through extinction of larger species and speciation of smaller species [83].…”

“…Although not originating at the same time, the diversification trajectories of all families show accelerated diversification at their origins, or in the case of the Braarudosphaeraceae, during their recovery following survival of the K-Pg extinction event (Figure 6b). Diversification trajectories following these initial "bursts" vary over time, and may correlate to different eco-physiological adaptive strategies under concurrent environmental forcings, such as the coccolith (and cell) size reductions in relation to long-term, global cooling [83]. This analysis also highlights that the Noelaerhabdaceae appear to be the only family that are in a current trajectory of adaptive radiation, whereas all others are in a state of "stationary clade growth" (Coccolithaceae and Calcidiscaceae) or seemingly at the final stages of a steady decline (Braarudosphaeraceae).…”

“…It will be important to (re-)investigate time series of phenotypic change in terms of rates of mean trait divergence and variations in concurrent environmental selection pressures. When comparing the different coccolithophore families and long-lived lineages, such as Calcidiscus [104] and Helicosphaera [83] in combination with genome-based and population genetic theory approaches [57,87], we may soon be able to explore these processes across the diversity of coccolithophores and perhaps derive a more unifying model for phenotypic change and speciation in this phytoplankton group. Such models may also provide better insights into how speciation (and extinction) rates may be affected by the current and future rapid rises in ocean temperature.…”

A new method for isolating and analysing coccospheres within sediment

“…ISX +PL enables rapid processing of down-core sediment samples or high spatial coverage from surface sediments allowing detection of high-resolution temporal or spatial changes in coccosphere size, and estimates of cell size. Cell size is an important parameter that enables us to examine the evolution and ecology of coccolithophore communities 11 , 44 , 45 . Temporal trends in cell size provide a record of micro- and macroevolution, for example, the reduction in size (stunting or dwarfing) immediately following extinction (Liliput effect 46 ) and the general radiation towards a larger cell size following speciation events (Cope’s Rule 47 ).…”

Adaptations of Coccolithophore Size to Selective Pressures During the Oligocene to Early Miocene High CO2 World

“…Due to their small size, coccoliths can be recovered in very high abundances from Jurassic, Cretaceous, and Cenozoic sediments, often with original morphologies well preserved that can be used to reconstruct long‐term records of coccolithophore cell‐size down to the species level. These coccolithophore cell‐size records are now being utilized to better understand the long‐term evolution of this key physiological and ecological parameter in response to past environmental change on million‐year time scales over the Cenozoic (Alvarez et al, 2019; Hannisdal et al, 2012; Herrmann & Thierstein, 2012; Šupraha & Henderiks, 2020), especially within the genus Reticulofenestra (Henderiks & Pagani, 2007; Pagani et al, 2011; Young, 1990), ancestor of the predominant modern calcifying haptophytes Emiliania and Gephyrocapsa .…”