Box Dating origins

There was a sensation in 1996 when Greg Wray of Duke University and colleagues announced new molecular evidence that animals had diversified about 1200 Ma. This estimate predated the oldest animal fossils by about 600 myr. In other words, the molecular time scale seemed to be double the fossil age. This proposal suggested three consequences: (i) the Precambrian fossil record of animals (and presumably all other fossils) was even more deficient than had been assumed; (ii) the Cambrian explosion, normally dated at 542 Ma, would shift back deep into the Proterozoic; and (iii) all other splitting dates in the UTL (see Fig. 8.4) would have to be pushed back deeper into the Proterozoic and Archaean.

Wray's view was confirmed by a number of other molecular analyses of basal animal groups, but also of plants, Archaea and Bacteria. Their work is based on gene sequencing from RNA of the nucleus, and it is calibrated against geological time using some fixed points based on known fossil dates. The molecular clock model of molecular evolution (see p. 133) suggests that genes mutate at predictable rates through geological time, so if one or more branching points in the tree can be fixed from known fossil dates, then the others may be calculated in proportion to the amount of gene difference between any pair of taxa.

In Wray's case, mainly vertebrate dates were used, the assumed dates of branching between different groups of fishes and tetrapods in the Paleozoic. So, he had to extrapolate his dates from the Paleozoic fixed points back into the Precambrian. Extrapolation (fixing dates outside the range) is tougher than interpolation (fixing dates within a range between a known date and the present day): small errors on those Paleozoic dates would magnify up to huge errors on the Precambrian estimates.

Wray's calculations were criticized by Ayala et al. (1998), who recalculated a date of 670 Ma for the basal radiation of animals, much more in line with the fossil record. In a further revision, Kevin Peterson and colleagues from Dartmouth University (2004) showed that Wray had unwittingly found a very ancient date because vertebrate molecular clocks tick more slowly than those of most other animal groups. So, if vertebrate clocks are slower, it takes longer for a certain amount of genome change to occur than in other animals, and so any calibrations extrapolated from such dates will be much more ancient than they ought to be. Peterson et al. (2004) brought the date of divergence of bilaterian animals down to 573-656 Ma, and so the split of all animals would be just a little older, in line with Ayala et al.'s (1998) estimate.

The reconsideration of molecular clock methods has now opened the way for a great number of studies of the dating of other parts of the UTL (see Fig. 8.4). Most analysts accept a baseline date of 3.5-3.8 Ga for the universal common ancestor, the first living thing on Earth. For example, Hwan Su Yoon and colleagues (2004) from the University of Iowa were able to reconstruct a tree of photosynthetic eukaryotes, the various algal groups, as well as plants (Fig. 8.10), and to date it. They used fixed dates for the origin of life, the oldest bangiophyte red alga (see Box 8.3), the first green plants on land, the first seed plants, and higher branching points among gymnosperms and angio-sperms (see pp. 498, 501). These then allowed the team to date splits among marine algae around 1.5 Ga, in line with fossil evidence, and a major radiation of photosynthetic eukaryotes from 1.0 Ga onwards. Their dates also give information on the timing of some events in the endosymbiotic model for the acquisition of organelles by green plant cells (Fig. 8.10).

Read more about the three-domain tree of life at http://www.blackwellpublishing.com/ paleobiology/.

Bangiomorpha Pubescens

Figure 8.10 Diagram showing the evolutionary relationships and divergence times for the red, green, glaucophyte and chromist algae. These photosynthetic groups are compared with the Opisthokonta, the clade containing animals and fungi. The tree also shows two endosymbiotic events. Some time before 1.5 Ga, the first such event took place, when a photosynthesizing cyanobacterium (CB) was engulfed by a eukyarote. The second endosymbiotic event involved the acquisition of a plastid about 1.3 Ga. Plastids in plants store food and may give plants color (chloroplasts are green). (Courtesy of Hwan Su Yoon.)

Figure 8.10 Diagram showing the evolutionary relationships and divergence times for the red, green, glaucophyte and chromist algae. These photosynthetic groups are compared with the Opisthokonta, the clade containing animals and fungi. The tree also shows two endosymbiotic events. Some time before 1.5 Ga, the first such event took place, when a photosynthesizing cyanobacterium (CB) was engulfed by a eukyarote. The second endosymbiotic event involved the acquisition of a plastid about 1.3 Ga. Plastids in plants store food and may give plants color (chloroplasts are green). (Courtesy of Hwan Su Yoon.)

scopic acritarchs, marine plant-like organisms (see p. 216) that are known from rocks dated 1.45 Ga.

Eukaryotes may be identified by their nuclei, and paleontologists have hoped to find such clinching evidence in the fossils. For a time, many believed that nuclei had been identified in the diverse eukaryotes from the much younger Bitter Springs Cherts of central Australia, dated at about 800 Ma. Some cells show apparent nuclei (Fig. 8.11b), but the dark areas probably only represent condensations of the cell contents. The Bitter Springs fossils also show evidence of cell division, but what kind of cell division?

Normal cell divisions in growth are called mitosis, where all the cell contents, including the DNA, are shared. Mitosis is seen in asexual and sexual organisms. The globular Gleno-botrydion from the Bitter Springs Chert shows cells in different stages of mitotic division (Fig. 8.11b), where one cell divides into two, and then the two divide into four. Eotetrahe-drion (Fig. 8.11c), once described as a reproducing eukaryote, is now interpreted as a cluster of cyanobacteria. Other fossils include

Spore tetrads Septum

Nucleus.

Nucleus.

New cell wall

Branched tubular filament

Branched tubular filament

Spore tetrads Septum

Figure 8.11 Early fossil "eukaryotes". (a) The thread-like Grypania meeki, preserved as a carbonaceous film, from the Greyson Shale, Montana (c. 1.3 Ga). (b, c) Single-celled eukaryotes from the Bitter Springs Chert, Australia (c. 800 Ma): (b) Glenobotrydion showing possible mitosis (cell division in growth), and (c) Eotetrahedrion, probably a cluster of individual Chroococcus-like cyanobacteria. (d) Branching siphonalean-like filament. Scale bars: 2 mm (a), 10 |im (b-d). (Courtesy of Martin Brasier, based on various sources.)

branched filaments that look like modern siphonalean green algae (Fig. 8.11d).

Older fossils too look like algae. For example, in the Lakhanda Group of eastern Siberia, 1000-950 Ma, five or six metaphyte species have been found (Fig. 8.12), as well as a colonial form that forms networks rather like a slime mold. But the key fossil in understanding early eukaryote evolution is Bangio-morpha (Box 8.3).

Multicellular^ and sex_

As eukaryotes ourselves, multicellularity and sex seem obvious. Prokaryotes are single-celled organisms, although some form filaments and loose "colonial" aggregations. True multicellular organisms arose only among the eukaryotes. These are plants and animals that are composed of more than one cell, typically a long string of connected cells in early forms. Multicellularity had several important consequences, one of which was that it allowed plants and animals to become large (some giant seaweeds or kelp, forms of algae, reach lengths of tens of meters). Another consequence of multicellularity was that cells

Figure 8.12 A filamentous alga from the Lakhanda Group, Siberia (c. 1000 Ma), 400 |m wide. (Courtesy of Andy Knoll.)

could specialize within an organism, some being adapted for feeding, others for reproduction, defense or communication.

But it seems that multicellularity required sex as well. The first organisms almost certainly reproduced asexually, that is, their cells divided and split. Asexual reproduction, or budding as it is sometimes called, is really just a form of growth: cells feed and grow in size, and when they are big enough they split by mitosis to form two organisms. The DNA splits at the same time and is shared by the two new cells. Sexual reproduction, on the other hand, involves the exchange of gametes

(sperms and eggs) between organisms. Typically, the male provides sperm that fertilize the egg from the female. Gametes have half the normal DNA complement, and the two half DNA sets zip together to produce a different genome in the offspring, but clearly sharing features of father and mother. In eukaryotes, the DNA exists as two copies, each strand forming one half of the double-helix structure. Cell divisions in sexual reproduction are called meiosis, where the DNA unzips to form two single copies, one going into each gamete, prior to fusion after fertilization.

Box 8.3 Bangiomorpha: origin of multicellularity and sex

Red algae (rhodophytes) today range from single cells to large ornate plants, and they may be tolerant of a wide variety of conditions. The modern red alga Bangia, for example, can survive in a full range of salinities, from the sea to freshwater lakes. The oldest fossil red alga was announced in 1990, and described in detail by Nick Butterfield from the University of Cambridge in 2000. The specimens are preserved in silicified shallow marine carbonates of the Hunting Formation, eastern Canada, dated at 1.2 Ga, together with a variety of other fossils, both prokaryote and eukaryote.

In his 2000 paper, Butterfield quippishly named the new form Bangiomorpha pubescens, the species name pubescens chosen "with reference to its pubescent or hairlike form, as well as the connotations of having achieved sexual maturity". The name Bangiomorpha pubescens has even made it into the dictionaries of bizarre and cheeky names; one web site notes "The fossil shows the first recorded sex act, 1.2 billion years ago. The 'bang' in the name was intended as a euphemism for sex." The fossils do not show sex acts, and the commentators surely exaggerate: Nick Butterfield may be based at the University of Cambridge in England, home of smutty humor since medieval times (if not before), but he is Canadian by birth!

Bangiomorpha grew in tufts of whiskery strands attached to shoreline rocks by holdfast structures made from several cells (Fig. 8.13a). The individual filaments are up to 2 mm long, and the cells are less than 50 |im wide. The cell walls are dark and enclose circular to disk-like cells, and the whole plant is enclosed in a further thick external layer. The individual filaments may be composed of a single series of cells, or of several series running side by side, or a combination of the two (Fig. 8.13b). Multiple-series filaments are composed of sets of wedge-shaped cells that radiate from the midline of the strand, a diagnostic feature of the modern Bangia and of all so-called bangiacean red algae.

Many dozens of specimens of Bangiomorpha have been found, and these show how the filaments developed. Starting with a single cell, the filament grew by division of cells (mitosis) along the filament axis. One cell divided into two, then two into four, and so on. Along the filaments (Fig. 8.13b), disk-shaped cells occur in clusters of two, four or eight, and these reflect further cell divisions within the filament. Some broader filaments show clusters of spherical, spore-like structures at the top end; if correctly identified, these prove that sexual reproduction and meiosis were taking place. Close study of the filaments, and of series of developmental stages, shows that Bangiomorpha was not only multicellular but that it showed differentiation of cells (holdfast cells versus filament cells), multiple cycles of cell division, differentiated spores and sexually differentiated whole plants.

Read more about Bangiomorpha in Butterfield's (2000) paper and at http://www. blackwellpublishing.com/paleobiology/.

Figure 8.13 The oldest multicellular eukaryote, Bangiomorpha, from the 1.2 Ga Hunting Formation of Canada. (a) A colony of whiskery filaments growing from holdfasts attached to a limestone base. (b) A single filament showing a single-series filament making a transition to multiple series, with sets of four wedge-shaped cells; note the sets of four disk-shaped cells in the single-series part of the strand. (Courtesy of Nick Butterfield.)

Figure 8.13 The oldest multicellular eukaryote, Bangiomorpha, from the 1.2 Ga Hunting Formation of Canada. (a) A colony of whiskery filaments growing from holdfasts attached to a limestone base. (b) A single filament showing a single-series filament making a transition to multiple series, with sets of four wedge-shaped cells; note the sets of four disk-shaped cells in the single-series part of the strand. (Courtesy of Nick Butterfield.)

Whereas some of the Bitter Springs Chert fossils were once supposed to show meiotic cell division, and so sex, this is now doubted. Must paleontologists find fossils of early eukaryotes actually engaged in sexual reproduction in order to prove the origin of sex? The answer is no, and a phylogenetic argument is enough. If we know that all species in a modern clade show sexual reproduction, then their ancestors probably did too. Many modern algae show sexual reproduction, and the oldest member of a sexually reproducing group is a 1.2 Ga red alga (see p. 200), so that provides a minimum date for the origin of sex.

One of the oldest multicellular organisms is Bangiomorpha (Box 8.3), obviously multicel-lular and a member of a modern group that engages in sex. Multicellularity allowed many new forms to appear. The term "algae" refers to a paraphyletic assortment of single-celled and multicelled organisms, all of them eukary-otes, and most of them photosynthetic. The major groups are distinguished by their color, morphology and biochemical properties.

Molecular phylogenies (see Fig. 8.4) show that many lines of eukaryotes have traditionally been termed "algae". Several algal groups now seem to be closely related to true plants (see p. 483). The fossil record of algae is patchy, but exceptions are the biostratigraphically useful dinoflagellates, coccoliths and diatoms, and calcareous algae such as dasycladaceans, charophytes and corallines (see p. 221).

Why have sex? Budding seems to be efficient enough, and it is what Bacteria, Archaea and many simple eukaryotes have always done, and continue to do today. The benefits are that the process is quick and efficient: what could be better for a successful organism than to replicate identical clones of itself? Sex, on the other hand, is a messy and complex business. Many simple organisms, and even fishes and amphibians, produce vast numbers of eggs, sometimes millions that are shed into the water, where most are wasted. Sperm of course is also produced in vast quantities, and most goes to waste. Nonetheless, the invention of sex is usually seen as one of the great milestones in biological evolution (see p. 546).

The reason for its origin may be obscure, but its consequences are manifest. Sex allows rapid evolution and diversification of species because genetic material is swapped and changes during each reproductive cycle. Sexual organisms vary more than asexual organisms, and they can adapt and specialize more readily. Finally, sexual organisms can be multicellular.

The Late Neoproterozoic_

The last 100 myr of the Proterozoic, the Late Neoproterozoic, is marked by a dramatic increase in fossil diversity. Sexual reproduction and multicellularity opened the door for more complex, and larger, organisms. Algal groups, including relatives of plants, appeared. In addition, multicellular animals or metazoans, also appeared later in the Proterozoic, and these included the complex Ediacaran animals.

1 Find out how many distinct creation myths you can track down on the internet. Arrange them in a classification that links major features of the myths, and match them to their appropriate religions and time span of general acceptability.

2 Many claims have been made over the years about the oldest fossils of life. Look back through the literature to find what was the oldest acceptable record in 1960, 1970, 1980, 1990 and 2000. Read about why many of these claimed oldest finds were eventually doubted or rejected, and list the reasons why.

3 Read around the debate about the universal tree of life, and consider whether it will ever be possible to determine which branched first - Archaea, Bacteria or Eucarya - and give reasons why some analysts believe that this will never be resolved.

4 What are the advantages and disadvantages of sex and of multicellularity? Catalog as many arguments as you can find for and against each of these biological attributes, and describe the possible world today if sex and multicellularity had never arisen.

5 Why are fossils so rare in the Precambrian?

Further reading

Butterfield, N.J. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/ Neoproterozoic radiation of eukaryotes. Paleobiol-ogy 26, 386-404.

Cavalier-Smith, T., Brasier, M. & Embley, T.M. (eds) 2006. How and when did microbes change the world? Philosophical Transactions of the Royal Society B 361, 845-1083.

Cracraft, J. & Donoghue, M.J. (eds) 2004. Assembling the Tree of Life. Oxford University Press, Oxford, UK.

Hazen, R. 2005. Genesis: The Scientific Quest for Life's Origin. Joseph Henry Press, Washington. http:// darwin.nap.edu/books/0309094321/html/.

Knoll, A.H. 1992. The early evolution of eukaryotes: a geological perspective. Science 256, 622-7.

Knoll, A.H. 2003. Life on a Young Planet: The First Three Billion Years of Evolution on Earth. Princeton University Press, Princeton, NJ.

Tudge, C.T. 2000. The Variety of Life. Oxford University Press, Oxford, UK.

References

Altermann, W. & Kazmierczak, J.2003. Archean microfossils: a reappraisal of early life on Earth. Research in Microbiology 154: 611-17.

Ayala, F.J., Rzhetsky, A.& Ayala, F.J. 1998. Origin of the metazoan phyla: molecular clocks confirm pale-ontological estimates. Proceedings of the National Academy of Sciences, USA 95, 606-11.

Barghoorn, E.S. & Taylor, S.A. 1965. Microorganisms from the Gunflint Chert. Science 147, 563-77.

Baldauf, S.L., Bhattacharya, D., Cockrill, J., Hugenholtz, P., Pawlowski, J. & Simpson, A.C.B. 2004. The tree of life, an overview. In Cracraft, J. & Donoghue, M.J. (eds) Assembling the Tree of Life. Oxford University Press, Oxford, UK, pp. 43-75.

Brasier, M.D., Green, O.R., Jephcoat, A.P. et al. 2002. Questioning the evidence for earth's oldest fossils. Nature 416, 76-81.

Brocks, J.J., Logan, G.A., Buick, R. & Summons, R.E. 1999. Archean molecular fossils and the early rise of Eukaryotes. Science 285, 1033-6.

Butterfield, N.J. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/ Neoproterozoic radiation of eukaryotes. Paleobiol-ogy 26, 386-404.

Catling, D.C. & Claire, M. 2005. How Earth's atmosphere evolved to an oxic state: a status report. Earth and Planetary Science Letters 237, 1-20.

Review questions

Ciccarelli, F.D., Doerks, T., von Mering, C. et al. 2006. Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283-7.

Crick, F.H.C. 1968. The origin of the genetic code. Journal of Molecular Biology 38, 367-9.

Doolittle, W.F. & Bapteste, E. 2007. Pattern pluralism and the Tree of Life hypothesis. Proceedings of the National Academy of Sciences, USA 104, 243-9.

Embley, T.M. & Martin, W. 2006. Eukaryotic evolution, changes and challenges. Nature 440, 623-30.

Gilbert, W. 1986. The RNA world. Nature 319, 618.

Mclnerney, J.O., Cotton, J.A. & Pisani, D. 2008. The prokaryotic tree of life: past, present . . . and future? Trends in Ecology and Evolution 23, 276-81.

Nisbet, E.G. & Sleep, N.H. 2001. The habitat and nature of early life. Nature 409, 1083-91.

Peterson, K.J., Lyons, J.B., Nowak, K.S. et al. 2004. Estimating metazoan divergence times with a molecular clock. Proceedings of the National Academy of Sciences, USA 101, 6536-41.

Poole, A.M. & Penny, D. 2007. Evaluating hypotheses for the origin of eukaryotes. BioEssays 29, 7484.

Rasmussen, B. 2000. Filamentous microfossils in a 3,235-million-year-old volcanogenic massive sulfide. Nature 405, 676-9.

Rosing, M.T. & Frei, R. 2004 U-rich Archean sea-floor sediments from Greenland - indications of >3700 Ma oxygenic photosynthesis. Earth and Planetary Science Letters 217, 237-44.

Schopf, J.W. 1993. Microfossils of the Early Archean Apex Chert: new evidence of the antiquity of life. Science 260, 640-6.

Schopf, J.W., Kudryavtsev, A.B., Agresti, D.G., Wdowiak, T.J. & Czaja, A.D. 2002. Laser-Raman imagery of Earth's earliest fossils. Nature 416, 73-6.

Schopf, J.W. & Packer, B.M. 1987. Early Archean (3.3-billion to 3.5 billion-year-old) microfossils from Warrawoona Group, Australia. Science 237, 70-3.

Szostak, J.W., Bartel, D.P. & Luisi, P.L. 2001. Synthesizing life. Nature 409, 387-90.

Whittaker, R. 1969. New concepts of kingdoms or organisms: evolutionary relations are better represented by new classifications than by the traditional two kingdoms. Science 163, 150-60.

Woese, C.R. & Fox, G.E. 1977. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proceedings of the National Academy of Sciences, USA 74, 5088-90.

Wray, G.A., Levinton, J.S. & Shapiro, L. 1996. Molecular evidence for deep pre-Cambrian divergences among the metazoan phyla. Science 274, 568-73.

Yoon, H.S., Hackett, J.D., Ciniglia, C., Pinto, G. & Bhattacharya, D. 2004. A timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution 21, 809-18.

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