Repeated species radiations in the recent evolution of the key marine phytoplankton lineage Gephyrocapsa

Abstract

Phytoplankton account for nearly half of global primary productivity and strongly affect the global carbon cycle, yet little is known about the forces that drive the evolution of these keystone microscopic organisms. Here we combine morphometric data from the fossil record of the ubiquitous coccolithophore genus Gephyrocapsa with genomic analyses of extant species to assess the genetic processes underlying Pleistocene palaeontological patterns. We demonstrate that all modern diversity in Gephyrocapsa (including Emiliania huxleyi) originated in a rapid species radiation during the last 0.6 Ma, coincident with the latest of the three pulses of Gephyrocapsa diversification and extinction documented in the fossil record. Our evolutionary genetic analyses indicate that new species in this genus have formed in sympatry or parapatry, with occasional hybridisation between species. This sheds light on the mode of speciation during evolutionary radiation of marine phytoplankton and provides a model of how new plankton species form.

Shifts in Phytoplankton Composition and Stepwise Climate Change During the Middle Miocene

“…Diversification pulses within the Noelaerhabdaceae, characterized by a gradual increase in maximum sizes and terminated by abrupt declines in size, have been documented across the Neogene (e.g., Beaufort, 1992; 10.1029/2020PA003915 Bollmann et al, 1998;Bolton et al, 2016;Henderiks & Pagani, 2007;Imai et al, 2015;Matsuoka & Okada, 1990;Young, 1990). Recently, Bendif et al (2019) demonstrated that such pulses reflect species radiations (speciation) separated by abrupt extinctions and that the three most recent pulses in the Pleistocene evolution of Gephyrocapsa (including E. huxleyi) are associated with step changes in global SST. These Pleistocene bursts in species diversification ("Matsuoka-Okada cycles") had durations of~0.5 Myr (Bendif et al, 2019), much shorter than those suggested by the Miocene data sets (e.g., Henderiks & Pagani, 2007;Imai et al, 2015;Young, 1990; this study).…”

“…Recently, Bendif et al (2019) demonstrated that such pulses reflect species radiations (speciation) separated by abrupt extinctions and that the three most recent pulses in the Pleistocene evolution of Gephyrocapsa (including E. huxleyi) are associated with step changes in global SST. These Pleistocene bursts in species diversification ("Matsuoka-Okada cycles") had durations of~0.5 Myr (Bendif et al, 2019), much shorter than those suggested by the Miocene data sets (e.g., Henderiks & Pagani, 2007;Imai et al, 2015;Young, 1990; this study). This could be due to a true acceleration of evolutionary rates (and related climatic forcings) during the Pleistocene compared to the Miocene.…”

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

“…6c). A prime example of this is the comparison between the Helicosphaera genus, with its highly conserved morphology, little phenotypic innovation, low abundances and relatively stable biogeochemical performance; and the Noelaerhabdaceae, with the potential for inter-species hybridization (Bendif et al, 2015) and rapid diversification (Bendif et al, 2019), global dominance in marine phytoplankton communities (Suchéras-Marx and Henderiks, 2014; Fig. S3) and a range of possible biogeochemical outputs ( Fig.…”

The Genetic Basis of Scale-Loss Phenotype in the Rapid Radiation of Takifugu Fishes

“…To observe the developmental pattern of scales in Takifugu species, three closely-related species, one scale-covered (T. niphobles) and two scale-uncovered (T. pardalis and T. snyderi), were obtained by in vitro fertilization and sampled at 1,2,3,5,7,14,21,28,29,56,63, and 101 days post-hatch (dph). Live fish were stained up to 63 dph with 0.1% alizarin red S or 2% cochineal dye (Kiriya Chemical, Osaka, Japan) dissolved in half-strength seawater for 8 hours, washed in half-strength seawater for 10 min, and then euthanized in ice-cold seawater.…”

“…Classic examples of the rapid radiation include finch birds, silversword plants, anole lizards, threespine sticklebacks, and cichlid fishes [1][2][3][4][5][6]. Recent advances in genomics have enabled the study of the genetic basis of phenotypic evolution associated with rapid adaptation not only in the classic examples but also in many other groups of organisms [7,8]. Interestingly, this line of research also allows investigations into the predictability of evolutionary change [9][10][11][12][13].…”