Elsevier

Journal of Environmental Sciences

Volume 63, January 2018, Pages 218-226
Journal of Environmental Sciences

Opinion discussion
Reactive oxygen species may play an essential role in driving biological evolution: The Cambrian Explosion as an example

https://doi.org/10.1016/j.jes.2017.05.035Get rights and content

Abstract

The Cambrian Explosion is one of the most significant events in the history of life; essentially all easily fossilizable animal body plans first evolved during this event. Although many theories have been proposed to explain this event, its cause remains unresolved. Here, we propose that the elevated level of oxygen, in combination with the increased mobility and food intake of metazoans, led to increased cellular levels of reactive oxygen species (ROS), which drove evolution by enhancing mutation rates and providing new regulatory mechanisms. Our hypothesis may provide a unified explanation for the Cambrian Explosion as it incorporates both environmental and developmental factors and is also consistent with ecological explanations for animal radiation. Future studies should focus on testing this hypothesis, and may lead to important insights into evolution.

Introduction

Although the first animals may have evolved during the Ediacaran Period (about 580 million years ago (mya)) or even earlier, essentially all easily fossilizable animal body plans emerged within about 35 mya in the early Cambrian (Marshall, 2006, Briggs, 2015, Valentine, 2004, Butterfield, 2015). This phenomenon is called the Cambrian Explosion, and is one of the most important evolutionary events in Earth history.

There have always been questions about the reliability of fossil evidence, because of the incompleteness of the fossil record and conflicts with molecular clock estimates. However, recent evidence strongly supports the conclusion that the Cambrian Explosion was a real evolutionary phenomenon as opposed to an artifact of taphonomy. The occurrence of trace fossils is independent of the presence of hard parts, and can provide information on soft-bodied animals that were rarely preserved. Studies have shown that trace fossils became larger and more complex throughout the Cambrian Period, which is consistent with the rapid radiation of animals (Valentine, 2004). Although earlier molecular clock analyses often conflicted with fossil data by suggesting many phyla evolved several hundred million years before the Cambrian, recent advances in molecular analyses have significantly reduced Precambrian divergence time estimates between phyla (Lee et al., 2013, Erwin et al., 2011, Rota-Stabelli et al., 2013), and current results from molecular analyses and are more or less reconcilable with the fossil record.

One explanation for the Cambrian Explosion is that the rate of animal evolution may have been much higher during that period. One simulation study has indicated that rates of evolution would have to increase by a factor of five to recreate the observed divergences that were then compressed into 35 million years (Levinton et al., 2004). Recent analyses of molecular and morphological data of arthropods have suggested that their rates of evolution indeed increased by 4- to 5.5-fold in the early Cambrian (Lee et al., 2013).

Several possible mechanisms for the Cambrian explosion have been proposed (Marshall, 2006, Valentine, 2004); some are based on environmental changes, such as increased atmospheric oxygen levels or Snowball Earth events. However, it is difficult to directly correlate environmental change with new levels of developmental and morphological organization. Another theory is that the evolution of a new genetic circuit was the primary cause. However, evidence suggests that the genes governing bilaterian development evolved at least tens of millions years before the Cambrian Explosion (Valentine, 2004). Finally, there are ecological explanations whereby predation and grazing are suggested to have been the major causes of the rapid radiation of animals. Although ecological factors are expected to play important roles in evolution, these theories fail to explain the duration and uniqueness of the Cambrian Explosion. Furthermore, none of these theories directly address why the rate of evolution increased.

It has long been established that oxygen can produce reactive oxygen species (ROS), and that the resulting oxidative stress may cause genomic damage and mutations (Schieber and Chandel, 2014, Puente et al., 2014, Cadet and Wagner, 2013). Furthermore, because ROS are also important signaling molecules, their increased abundance could also provide new regulatory mechanisms for development (Covarrubias et al., 2008). Therefore, we proposed that ROS may have been a central factor in the environmental, developmental and ecological mechanisms that caused the radiation of early bilaterians. In the following sections of this article, we will discuss this model in greater detail.

Section snippets

Increased oxygen level before the Cambrian set the stage for animal evolution

Before the Great Oxygenation Event (GOE) at about 2.45 Ga, any oxygen molecules in the atmosphere were captured by oxygen sinks such as dissolved iron and organic matter (Canfield, 2005, Canfield, 1998, Holland, 2006). Between 1.8 and 0.85 Ga, the oxygen level in the atmosphere remained low, no more than 10% PAL (present atmospheric level) (Canfield, 2005, Canfield, 1998, Holland, 2006, Sperling et al., 2015, Mills and Canfield, 2014). Some researchers have estimated that during much of the

Increased oxygen consumption generates more ROS and contributes to evolution

ROS include a series of reactive compounds, such as superoxide anions (O2radical dot), hydroperoxyl radicals (HO2radical dot), hydrogen peroxide (H2O2), and hydroxyl radicals (radical dotOH), all of which are derived from the reduction of molecular oxygen. The primary ROS is the superoxide anion (O2radical dot), which is continuously produced as a byproduct of the mitochondrial electron transport chain (Sabharwal and Schumacker, 2014, Fisher-Wellman and Bloomer, 2009) (Fig. 1). Superoxide anions are generally converted to hydrogen

Global environmental disturbances causing large-scale ecological oxidative stress

The well-documented presence of unusually large negative carbon isotopic excursions at the Neoproterozoic–Cambrian boundary points to environmental disturbances (Knoll and Carroll, 1999). One possible cause is that the relatively rapid movement of continents may have led to immense methane burps that induced significant temperature increases (Kirschvink and Raub, 2003, Peters and Gaines, 2012). Furthermore, a long period of oxygen erosion in the Neoproterozoic Era may have resulted in

ROS regulate key developmental genes and signaling pathways that affect cell renewal and differentiation

In addition to causing oxidative stress and producing mutations, ROS can also directly regulate the embryonic developmental process (Puente et al., 2014, Covarrubias et al., 2008, Brautigam et al., 2011). Some of the most important developmental genes, such as Hox, TGF-β, Otd, and Pax, initiate morphogenesis and are inferred to have been present in stem-group bilaterians (Covarrubias et al., 2008, Kamata et al., 2005). ROS play an important role in regulating these key genes. For example, Pax

The evolutionary lag between the digestive and excretory systems in early metazoans may also cause oxidative stress

The history of animal evolution is accompanied by constant improvement of the digestive tract (Valentine, 2004). For example, sponges and placozoans lack an enteron (Valentine, 2004). A primitive gut evolved in cnidarians. Triploblastslater evolved an increasingly sophisticated digestive system with two openings and digestive glands (Valentine, 2004, Vannier et al., 2014). In comparison, the evolution of the excretory system lagged behind significantly. For example, the acoel flatworm, the

An oxidative model for the evolution of early bilaterians

Here we propose a revised model for the Cambrian Explosion (Fig. 3). During the Ediacaran Period, oxygen levels at the bottom of shallow seas were elevated above a threshold sufficient to support larger and more active animals, which enabled the rise of the Ediacarabiota, some of which may have been triploblastic and possibly stem-group bilaterians. Because of the increased mobility of these animals, they would have consumed more oxygen and produced greater amounts of ROS. In addition, their

ROS may have broader implications in evolution

Evolution driven by ROS may explain other evolutionary events in addition to the Cambrian Explosion, including the origins of eukaryotes and insects.

Different models have been proposed to explain the origin of eukaryotes (Zimmer, 2009). The traditional “archezoa hypothesis” suggests a proto-eukaryotic cell that had already evolved a nucleus, a cellular skeleton and the endomembrane system before it acquired mitochondria through endosymbiosis. The major difficulty facing this model is the

Conclusions

We propose that ROS were important factors in driving the Cambrian Explosion. Several other factors, including rising oceanic oxygen levels and the appearance of primitive bilaterians that were more metabolically active and had improved digestive systems, could lead to the accumulation of ROS in tissues. Excess ROS can cause genomic mutations, which may increase the rate of evolution. In addition, ROS may have provided new regulatory mechanisms that were incorporated into the genetic circuit

Author disclosure statement

No competing financial interests exist.

Acknowledgments

This work was supported by the Program of Co-Construction with the Beijing Municipal Commission of Education of China and Fundamental Research Funds for the Central Universities (No. 2015KJJCB19).

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