Cyclic evolution of phytoplankton forced by changes in tropical seasonality

Abstract

The effect of global climate cycles driven by Earth's orbital variations on evolution is poorly understood because of difficulties achieving sufficiently-resolved records of past evolution. The fossil remains of coccolithophores, a key calcifying phytoplankton group, enable an exceptional assessment of the impact of cyclic orbital-scale climate change on evolution because of their abundance in marine sediments, and because coccolithophores demonstrate extreme morphological plasticity in response to the changing environment1,2. Recently, evolutionary genetic analyses linked broad changes in Pleistocene fossil coccolith morphology to species radiation events3. Here, using high-resolution coccolith data, we show that during the last 2.8 million years coccolithophore evolution was forced by Earth's orbital eccentricity with rhythms of ~100,000 years and 405,000 years -a distinct spectral signature to that of coeval global climate cycles4. Simulations with an Earth System Model5 including the marine carbon cycle6 demonstrate that eccentricity directly impacts the diversity of ecological niches occurring over the annual cycle in the tropical ocean. Reduced seasonality favours species with mid-size coccoliths that bloom yearround, increasing coccolith carbonate export and burial. We posit that eccentricity pacing of phytoplankton evolution contributed to the strong 405,000-year pacing seen in records of the global carbon cycle.

Rapid diversification underlying the global dominance of a cosmopolitan phytoplankton

“…Within A1, intra-specific divergences then occurred through different events of vicariance during the MIS4-2 glacial period, establishing genetically distinct populations along a latitudinal gradient. A significant eccentricity minimum associated with these events could account for interactions between newly diversified populations within A1 due to stronger compression of ecological niches [ 69 ]. In this scheme, gene-flow between emerging populations could have played a role in the adaptive process associated with expanded habitat to higher latitudes.…”

“…Gene flow events within A1 redistributed allelic composition associated with common ancestors of the three lineages into newly formed populations, contributing to potential adaptation to environmental variability along latitudinal gradients. The 400 ky cycle of the absolute eccentricity minimum, which had not occurred since the origin of the G. huxleyi lineage, may be related to major events of diversification within Gephyrocapsa [ 69 ].…”

Evolutionary Rates in the Haptophyta: Exploring Molecular and Phenotypic Diversity

“…However, it has long been recognized that key questions involving the molecular, morphological and physiological diversity of the group are best explored with combinations of expertise found within the fields of biology and earth sciences [171,172]. The promise of combining molecular techniques with detailed fossil time series data is exemplified in recent studies of E. huxleyi and its closest relatives [57,58,103]. Expanding this approach to include other key coccolithophore clades will be crucial in exploring the hypothesized differences in evolutionary rates or adaptive strategies between clades [83,173].…”

“…It was also shown that interspecific hybridization and gene exchange is a very recent phenomenon in these blooming coccolithophores [58], confirming that the group continues to diversify today, on the adaptive radiation trajectory that started in the latest Miocene-Pliocene [102] (see also Figure 6b). A second, alternative hypothesis involves a role of long (405,000 year) orbital cycles forcing the repeated pattern of size expansions and contractions within the Noelaerhabdaceae over the past 2.8 Myr [103]. The eccentricity of Earth's orbit around the sun influences seasonal contrasts, which in turn determine the phytoplankton seasonal succession and the number of available niches in the photic zone.…”

Morphometric changes in two Late Cretaceous calcareous nannofossil lineages support diversification fueled by long-term climate change

“…However, some analogy might be drawn in our understanding of how climate change affects biodiversity because, as recently demonstrated in the Quaternary, rapid phenotypic size changes in calcareous nannoplankton almost always imply speciation events, which appear to be related to significant climate changes (Bendif et al, 2019;Beaufort et al, 2022). Moreover, direct causal factors that can be invoked for size variation in plankton may be indirectly related to temperature and, in fact, driven by other factors, like fertility and light availability.…”