Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta)

Abstract

Summary Patterns of species richness are commonly linked to life history strategies. In diatoms, an exceptionally diverse lineage of photosynthetic heterokonts important for global photosynthesis and burial of atmospheric carbon, lineages with different locomotory and reproductive traits differ dramatically in species richness, but any potential association between life history strategy and diversification has not been tested in a phylogenetic framework.We constructed a time‐calibrated, 11‐gene, 1151‐taxon phylogeny of diatoms – the most inclusive diatom species tree to date. We used this phylogeny, together with a comprehensive inventory of first–last occurrences of Cenozoic fossil diatoms, to estimate ranges of expected species richness, diversification and its variation through time and across lineages.Diversification rates varied with life history traits. Although anisogamous lineages diversified faster than oogamous ones, this increase was restricted to a nested clade with active motility in the vegetative cells.We propose that the evolution of motility in vegetative cells, following an earlier transition from oogamy to anisogamy, facilitated outcrossing and improved utilization of habitat complexity, ultimately leading to enhanced opportunity for adaptive divergence across a variety of novel habitats. Together, these contributed to a species radiation that gave rise to the majority of present‐day diatom diversity.

Diatoms diversify and turn over faster in freshwater than marine environments*

“…The relatively high global extinction fraction ( ε = 0.8; Table ), estimated here from extant species only, was similar to calculations made from Cenozoic marine fossils (ε = 0.75; Nakov et al. ). Analyses using alternative implementations of the conditioning of survival of crown lineages indicated that the two approaches produce very similar results (Fig.…”

“…For example, the net diversification waiting time for marine planktonic lineages under the MuHiSSE model was 17 My in first and 2.7 My in the second hidden state, whereas the waiting time for oogamous nonmotile diatoms (most common in the marine plankton) was previously estimated as between 16.6 and 100 My (phylogenetic data) or roughly 34.5 My (fossil data) (Nakov et al. ). The relatively high global extinction fraction ( ε = 0.8; Table ), estimated here from extant species only, was similar to calculations made from Cenozoic marine fossils (ε = 0.75; Nakov et al.…”

“…We used a time‐calibrated phylogeny of 1151 diatoms reconstructed from a concatenated alignment of 11 genes (Nakov et al. )—the largest available phylogenetic tree of diatoms that covers their known phylogenetic and ecological breadth. We scored 1132 of the 1151 species for two characters: “habitat” (plankton or benthos) and “salinity” (marine or freshwater) based on taxonomic compilations (Round et al.…”

“…We used a time-calibrated phylogeny of 1151 diatoms reconstructed from a concatenated alignment of 11 genes (Nakov et al 2018)-the largest available phylogenetic tree of diatoms that covers their known phylogenetic and ecological breadth. We scored 1132 of the 1151 species for two characters: "habitat" (plankton or benthos) and "salinity" (marine or freshwater) based on taxonomic compilations (Round et al 1990;Hasle and Syvertsen 1996;Lange-Bertalot and Krammer 2000;Witkowski et al 2000;Lobban et al 2012) and previous work on character evolution (Alverson et al 2007;Nakov et al 2015;Ruck et al 2016).…”

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“…Due to constraints of our dataset, we were not able to reliably make inferences using hiSSE or fiSSE analyses (see ). Finally, to summarize diversification rates over time and with respect to each character state, we adopted the approach of Nakov, Beaulieu, and Alverson (): we binned the phylogeny into time‐intervals of 0.001 units, resampled the parameter estimates at each interval and then plotted the values by character state. Note that diversification rates are sensitive to the maximum tree depth and are inflated due to the relative time calibration in BEAST (); however, this should not affect conclusions drawn within the clade.…”