The inspiration for this book arises from the creation of the Origins Institute (OI) at McMaster University, which formally started operating in July 2004. Many of the greatest questions that face twenty-first century scientists are interrelated in fundamental ways. The OI was established to address several of these major interdisciplinary questions from within a broad framework of ‘origins’ themes: space-time, elements, structure in the cosmos, life, species, and humanity.

The origin of life has a privileged position in this great sweep of scientific endeavour and ideas. It addresses, arguably, the most surprising and most fundamental transition to have arisen during the entire evolution of the universe, namely, the transformation of collections of molecules from the inanimate to animate realm. Substantial progress in solving this great problem has been achieved relatively recently but may be traced back to ideas first proposed by Darwin. The great excitement in our era is the realization that physical properties of planetary systems play an important role in setting the stage for life, and that microbial life, on Earth at least, is incredibly robust and has adapted itself to surprisingly ‘extreme’ conditions. Progress can be traced to four scientific revolutions that have occurred over the last two decades:

1. the discovery, since 1995, of over 200 extrasolar planets (one which is only 7.5 times more massive than the Earth) around other stars and the possibility that at least a few of these systems may harbour life-sustaining planets;

2. the discovery of extremophile microorganisms on Earth that have adapted to conditions of extreme temperatures, acidity, salinity, etc., which considerably broadens the range of habitats where we might hope to find life on other planets in our solar system and other planetary systems;

3. […]

Introduction

The remnants of ancient life on Earth are extremely rare and difficult to interpret, since they have been modified by billions of years of subsequent geological history. Therefore, any understanding of the evolution of Earth's biosphere will heavily rely on the study of extant organisms for which complete genome sequences are already available or will eventually be established. A central point is the phylogenetic inference of the tree of life from such genomic data. Serving as a unifying framework, this tree will allow the disparate and often incomplete pieces of information gathered by various disciplines to be collected and structured. In the first half of this chapter, we will briefly explain the principles of phylogenetic inference and the major artefacts affecting phylogenetic reconstruction. Then we will introduce phylogenomics, starting with a theoretical presentation before illustrating the explained concepts through a case study centred on animal evolution. In the second half, we will review our present understanding of eukaryotic evolution and show how recent knowledge suggests that secondary simplification is an important mode of evolution that has been too long overlooked. We will also summarize the current views about the root and the shape of the tree of life. Finally, we will attempt to debunk two common hypotheses about the early evolution of life, i.e., a cell fusion at the origin of eukaryotes and a hyperthermophilic origin of life.

Introduction

Darwin was obsessed with origins. The book with which he distinguished himself as among the greatest thinkers ever to have walked on Earth, The Origin of Species by Means of Natural Selection or, The Preservation of Favoured Races in the Struggle for Life, was intended as only an abstract to a ‘big species book’ (Gould, 2002) about organisms and their environments and how they interact to elicit change over time. In a letter to Hooker (Darwin, 1871), Darwin speculated on how life, itself, might have originated, including the now infamous notion that it started in a ‘warm little pond’. As Einstein would do for physics with space and time less than a half-century later (Minkowski, 1952), Darwin, in his magnum opus and personal correspondence, accomplished for biology: ecology and evolution were inextricably linked forevermore.

But origins posed problems for Darwin, even concerning particular groups, such as metazoans (i.e., animals): ‘[t]here is another and allied difficulty, which is much graver. I allude to the manner in which numbers of species of the same group, suddenly appear in the lowest known fossiliferous rocks’ (Darwin, 1859; in the section titled ‘On the Imperfection of the Geological Record’).

In this chapter, we consider the origin of metazoans as a model for the origin of life. Considering only a group within the tree of life offers us three advantages in demonstrating our thesis (which is described in the subsequent paragraph).

Science is the midwife of metaphysics. However much it might protest that it confines itself to physical realities only, science cannot help but provoke metaphysical questions in the human mind. To be sure, when it confines itself to its own specialized sphere, each science is strictly physical, physical both in the scope of its investigation and in the results and data those investigations produce. But science's ultimate import is always metaphysical.

The problem of what exists: why this universe?

Einstein reportedly said: “What really interests me is whether God had any choice in the creation of the world”. What he meant by this informal remark was whether the physical universe must necessarily exist as it is or whether it could have been otherwise (or could have not existed at all). Today, almost all scientists believe that the universe could indeed have been otherwise; no logical reason exists why it has to be as it is. In fact, it is the job of the experimental scientist to determine which universe actually exists, from among the many universes that might possibly exist. And it is the job of the theoretician to construct alternative models of physical reality, perhaps to simplify or isolate a particular feature of interest. To be credible, these models must be mathematically and logically self-consistent. In other words, they represent possible worlds.

Let me give one example from my own research (Birrell and Davies, 1978). The equations of quantum field theory describing a system of interacting subatomic particles are often mathematically intractable. But several “toy models” exist, the equations for which may be solved exactly because of special mathematical features. One of these, known as the Thirring model, describes a two-spacetime-dimensional world inhabited by self-interacting fermions. This impoverished model of reality is designed to capture some features of interest to physicists in the real world. It is not, obviously, an attempt to describe the real world in its entirety.

Introduction

Any chemist looking at the molecular workings of a living cell from the vantage point of organic chemistry may have moments in which he desists from scientific business-as-usual and finds himself standing in awe before so much “molecular ingenuity” and sheer chemical beauty. If anyone, besides the biochemist, may be fit to recognize such marvels on the molecular level and put them into a proper perspective, it is the synthetic organic chemist, who tends to judge any new discovered molecular structure or process by the criterion of whether he could do such a thing himself: “If I had to, could I make this?” The question reflects a dichotomy, epistemological in nature, that has been with the science of organic chemistry from the very beginning: the two-fold task of studying molecules occurring in nature and creating by chemical synthesis molecules that have never existed before. Chemical synthesis has traditionally been the organic chemist's major tool for exploring the molecular world: the ability to synthesize molecules of ever-increasing complexity that mirror those produced by living nature has been a significant measure of progress in organic chemistry as a whole. Yet, the gap between what chemists are able to create by chemical synthesis and what nature achieves in biosynthesis remains immense.

Fortunately, it is inspiration rather than resignation that chemists are drawing from this gap, and they are encouraged to do so by considering how chemical thought and the chemist's ability to make molecules have changed in the course of the past two centuries.

How did life begin?

I (and most scientists) would answer, “By accident.” But what an absolutely unlikely accident it must have been! The earth on which life first appeared – prebiotic earth – was most inhospitable: a violent place, wracked by storms and volcanoes, wrenched by the pull of a moon that was much closer than the one we know now, still battered by cosmic impacts. On its surface and in its oceans were myriads of organic compounds, some formed in processes occurring on earth, some imported by infalls from space. Out of this universe of tumult and molecules, somehow a small subset of chemical processes emerged and accidentally replicated, thus stumbling toward what became the first cells. How could such a chaotic mixture of molecules have generated cells? Order usually decays toward disorder: Why do the tracks that led to life point in the opposite direction?

The origin of life is one of the biggest of the big questions about the nature of existence. Origin tends to occur frequently in these big questions: the origin of the universe, the origin of matter, the origin of life, the origin of sentience. We, scientists and non-scientists alike, have troubles with such “origins” – we were not there watching when the first events happened, we can never replicate them, and, when those first events happened, there was, in fact, no “we.”

Introduction

Kant (1755) and Laplace (1796) laid the foundations of our theory of planet formation, arguing that the Solar System formed in a flattened disk orbiting the Sun. Today we know such disks to be a part of the star formation process (see Chapter 4), and we have come a long way toward understanding the details of how a protostellar disk turns itself into planets. Most importantly, for ten years now we have been finding planets orbiting other stars; the current count of detected exoplanets exceeds 180, so that the Solar System now constitutes only a small minority of all known planets. The bad news is that Mercury, Venus, Earth, and Mars remain the only examples of terrestrial planets we know, since such bodies are still well below the mass threshold for detection around ordinary stars. Thus, apart from a pair of bodies orbiting the pulsar PSR1257 + 12 (Wolszczan and Frail, 1992), all known exoplanets are giants: gaseous bodies like Jupiter or Saturn with a couple of potentially Neptune-like examples recently added to the menagerie. However, impressive as the ‘king of the planets’ and its kind are, it is a terrestrial planet – a modest rocky body, three-thousandths Jupiter's mass – which actually harbours the life in our Solar System. And as we contemplate the possibility of life elsewhere in the Universe, it is inevitably upon terrestrial planets that we focus our attention.

Introduction

Every living organism is adapted to a specific growth temperature. In the case of humans, this is 37 °C and an increase by 5 °C becomes fatal. In the world of microbes, the growth temperature range is much more diverse: heat lovers (‘thermophiles’) grow optimally (fastest) at temperatures up to 65 °C (Brock, 1978; Castenholz, 1979). Since the time of Pasteur, it had been assumed generally that growing (vegetative) cells of bacteria were killed quickly by temperatures of 80 °C and above. The Pasteurization technology is based on this observation. In contrast, during the past few decades, hyperthermophiles (HT; Stetter, 1992) that exhibit unprecedented optimal growth temperatures in excess of 80 °C have been isolated (Stetter et al., 1981; Zillig et al., 1981; Stetter, 1982). HT turned out to be very common in hot terrestrial and submarine environments. In comparing the growth requirements of these present-day HT with the conditions on ancient Earth, similar organisms could or even should have existed already by Early Archaean times. Propelled by impact energy, microbes could have spread in between the planets and moons of the early Solar System. Is there any evidence for the existence of microbes at that time? Most likely, yes. But the recognition of ancient microfossils on the basis of morphology turned out to be difficult, leading to controversy. Nevertheless, there are chemical traces of life within rocks from Precambrian deep sea vents (Schopf et al., 1987; Brasier et al., 2002; van Zullen et al., 2002).

The boundaries of philosophy, science, and theology

Some of the deeper questions that humans have raised are not always answerable within the boundaries of science. Instead, philosophers and theologians have approached such questions within their own domains of competence. One such example is provided by the question of purpose in evolution (see the discussion below). Indeed, the concept of purpose in a general sense may be understood as something that one sets before oneself as an object to be attained, an aim to be kept, a plan to be formulated. In attempting to give an answer to the question of “purpose in nature,” we should discuss the main components of human knowledge in an integrated way, so as to ask the right questions in the right field of knowledge. This approach should encourage us to provide appropriate answers that are reasonable within philosophy, science, or theology. At this juncture, it may also be argued that the task of a scientist should be independent of those of the other areas of human culture (Russell, 1991, p. 13). On the other hand, it is surely useful to be aware that this view of the role of science that is “divorced” from both philosophy and natural theology can also be seen from a different point of view (Townes, 1995, p. 166): because science and religion are evolving and are similar in their search for truth, convergence of these independent searches for truth may occur in the future.

Our knowledge of the universe is steadily expanding. In large measure, this has been a result of radioastronomical observations. Among the most important is that the majority of the radiation of the universe is almost uniform and follows the spectral distribution of a thermal source at a temperature of 2.725 K. This cosmic background radiation is the remnant of the initial event, the Big Bang. Although this radiation is essentially uniformly distributed in the universe, the distribution of matter is highly non-uniform.

Matter, 99% hydrogen and helium, is found virtually entirely within galaxies. Galaxies occupy 10−7 of the volume of the universe, but contain most of the known matter. The origin of this separation of radiation and matter is a topic of much current study, as is the question of galaxy formation and the abundance and distribution of intergalactic matter. Although they are clearly fundamental to the question of the chemistry that occurs, it is not my intent or capability to discuss these most interesting questions (see Peebles, 1993). The heterogeneous distributions of matter occur universally. The average density within galaxies is 1 atom of hydrogen cm3, whereas outside of galaxies estimates are of less than 1 atom of hydrogen m3 in intergalactic regions. This sharp aggregation of matter means that the chemistry is occurring within galaxies. It is sensible to focus the discussion, therefore, primarily on the molecular abundances and the chemistry occurring in our galaxy, the Milky Way, because observations are much easier in view of the decrease of radiation intensity as the inverse square of the distance.

Introduction

Tracing organismal (species) histories on large evolutionary timescales remains a big challenge in evolutionary biology. Darwin metaphorically labelled these relationships the ‘tree of life’, but in his notebook he expressed unhappiness with this label, because in the ‘tree of life’ depicting species evolution only the tips of the branches are alive; this layer of living organisms rests on dead ancestors and extinct relatives. Darwin mused that therefore the term ‘coral of life’ would be more appropriate (B26 in Darwin (1987)); however, this alternative label did not gain popularity. Different markers have been utilized to elucidate the relationship among different lineages: from morphological characters to complete genomes. Since complete genomes are now available for organisms from all three domains of life, it is possible to use large amounts of data to attempt to decipher the relationships between all known organisms.

Many comparative genome analyses have shown that different genes in genomes often have different evolutionary histories (e.g., Hilario and Gogarten (1993), Nesbo et al. (2001), and Zhaxybayeva et al. (2004)), which implies that the tree of life metaphor (and a bifurcating tree as a model for evolutionary relationships in general) might be no longer adequate (Doolittle, 1999). The incongruence between gene histories can be attributed to many factors, one of which is horizontal gene transfer (HGT). Simulations based on coalescence have shown that HGT can affect not only the topology of an inferred phylogeny (and therefore inferences of last common ancestors), but also divergence times (Zhaxybayeva and Gogarten, 2004; Zhaxybayeva et al., 2005).

Learning from our own existence

Hoyle's [1] successful prediction of the 7.6 MeV resonance of the carbon-12 nucleus, based on observation of his own carbon-based existence, established the scientific usefulness of anthropic principles. These principles have become common, if not yet standard, tools in cosmology, where theories of initial conditions may not yet exist – or, if they do exist, may admit a range of values [2, 3, 4, 5, 6]. At the same time, anthropic principles have retained a traditional role in religion and philosophy, where sensitive dependence of human existence on laws of nature that could imaginably have been otherwise is interpreted as evidence for human significance in the creation of the universe.

The tendency of life forms to make universal use of, and seemingly to depend on, specific details of natural law or historical circumstance does not end with nuclear abundances. Following decades of studying the ways in which mammalian blood achieves homeostasis by exploiting favorable regions in carbonic-acid chemistry and similar adaptations, Henderson compiled a list of such dependences in physiology [7]. Inverting Darwin's description of selective fine-tuning of organisms for “fit” to their environments, Henderson characterized his physiological sensitivities anthropically as evidence of “the fitness of the environment” for life.

The rapid growth in understanding of biology, from structures to systems, seems likely to expose many more sensitivities of life to details of chemistry, physics, and history.