Adaptation to a Viscous Snowball Earth Ocean as a Path to Complex Multicellularity

Abstract

Animals, fungi, and algae with complex multicellular bodies all evolved independently from unicellular ancestors. The early history of these major eukaryotic multicellular clades, if not their origins, co-occur with an extreme phase of global glaciations known as the Snowball Earth.Here, I propose that the long-term loss of low viscosity environments due to several rounds global glaciation drove the multiple origins of complex multicellularity in eukaryotes and the subsequent radiation of complex multicellular groups into previously unoccupied niches. Under this scenario, life adapts to Snowball Earth oceans by evolving large size and faster speeds through multicellularity which acts to compensate for high viscosity seawater and achieve fluid flow at sufficient levels to satisfy metabolic needs. Warm, low viscosity seawater returned with the melting of the Snowball glaciers and with it, by virtue of large and fast multicellular bodies, new ways of life were unveiled. 2

Tonian Low‐Latitude Marine Ecosystems Were Cold Before Snowball Earth

“…In modern oceans, total biomass tends to be highest in coastal waters (Hatton et al., 2021; Jones et al., 2014; Laws et al., 2000) and this is also likely be true in the Precambrian (LaBarbera, 1978). The shift of shallow low‐latitude coastal environments from warm to cold with high viscosity during the late Tonian may have led to a diverse set of adaptive strategies including complex multicellularity (Simpson, 2021) and terrestrialization in algal lineages (Žárský et al., 2022). Rocks of a similar age and formed within similar depositional conditions to the Beck Spring Dolomite may therefore be important to understanding the lifestyles of the earliest complex multicellular life, including crown group metazoans (Erwin et al., 2011) and green algae (Del Cortona et al., 2020), prior to the initiation of Sturtian Snowball Earth.…”

Experimental Snowball Earth Viscosity Drives the Evolution of Motile Multicellularity

“…In this competitive environment, the novelty of becoming larger and moving faster in order to survive the cold, 2/6/24 Page 8 of 19 viscous conditions of Snowball Earth oceans would lead to an ecological innovation in the post-Snowball world. Nascent motile multicellular lineages could take advantage of low marine viscosities to manipulate their surroundings (55), feeding in new and previously inaccessible ways. The ability to control the local environment -as opposed to being subject to it -opened the door for the origin and specialization of the dominant multicellular lineages on Earth today.…”

“…With little observed extinction (54) and no spatial refugia (53), populations of Cryogenian unicellular eukaryotes must have adapted to the cold viscous conditions of Snowball Earth in order to overcome the 2/6/24 Page 5 of 19 metabolic deficit imposed on them. There are several hypothesized strategies that unicellular organisms could have used in order to minimize this deficit by optimizing size, motility, and metabolic scaling (55,56). Unicells could have become smaller, lowering their metabolic rates to match availability.…”

“…95% confidence intervals for molecular clock divergence time estimates for multicellular lineages (18, 19, 70). Body volume for fossils are split out by prokaryotes (bacteria and archaea), unicellular eukaryotes, and multicellular eukaryotes (17, 55). The earliest multicellular eukaryotic algae, Protocladus (21) and Bangiomorpha (71) are called out separately.…”

Temperature: a key driver of Earth's habitability over the last billion years

“…Support for the controlling effect of temperature-both the long-term cooling trend and shortterm fluctuations-on Earth's habitability through time comes from the fossil record in four forms: [1] a long-term cooling trend is supported by the microscopic body size of almost all taxa for much of the Neoproterozoic (see (65)). In the modern, high temperature environments limit the size of both larvae and adult ectotherms and endotherms; [2] both long-term cooling and short-term fluctuations in temperature are supported by the fact that macroscopic fauna appear first in deep water refugia, which likely experienced less temperature fluctuation and cooler overall temperatures (54,65,66). The first shallow water Ediacaran fossils appear after a 20-million year lag (Fig.…”