View - Kowalewski, M. - Virginia Tech

BENGTSON—ORIGINS AND EARLY EVOLUTION OF PREDATIONvariance during the course of evolution: if you startsmall and simple, the only direction to go is towardlarge and complex (Stanley, 1973b; Gould, 1988;Bonner, 1993, 1998). Thus any event ofdiversification is likely to bring with it an increasein variance and, hence, an average size increase.Two major advances in the early evolution oflife, however, are inseparably connected with sizeincrease: the origin of eukaryotes and the origin(s)of multicellularity. Both of these probably are infact direct results of predation.ORIGIN OF EUKARYOTESWhereas prokaryotic organisms (bacteria andarchea) represent almost all of the biochemicaldiversity of the biosphere, eukaryotic cells are thebasis for most of the structural and morphologicaldiversity, most particularly with regard tomulticellular organisms. In current theory,predation was a main factor behind the origin ofeukaryotes. Molecular and structural evidencesuggest that eukaryotes evolved through a seriesof endosymbiotic events in which prokaryotesengulfed or invaded other organisms, eventuallyleading to an amalgamation of several lineages intodaughter organisms representing a higher level ofco-operational complexity (Margulis, 1970, 1981;Cavalier-Smith, 1987a, 1987b; Martin and Müller,1998; Gray, 1999; Lang et al., 1999; Roger, 1999).In particular, mitochondria and chloroplasts,containing as they do their own genome, showstrong evidence of having been derived from freelivingα-proteocteria and cyanobacteria, respectively(Gray and Spencer, 1996). The probable origin ofthese endosymbiotic relationships is predation bymeans of phagocytosis and the survival of some preywithin the predator (McFadden et al., 1994; de Duve,1995; Roger, 1999). Thus the origin of eukaryotesmay be seen as a direct consequence of predatorialinteractions among prokaryotes (e.g., MaynardSmith and Szathmáry, 1995).The same may be true of the origin of eukaryoticsex. The classic interpretation of sex in eukaryotesis that it arose from a single organism as a means ofreshuffling genomes. Maynard Smith and Szathmáry(1995) propose that alternating meiosis andendomitosis in this organism produced a haploiddiploidlife cycle, and that (isogamous) syngamyeventually replaced endomitosis for the productionof the diploid phase (because of the doubleadvantages of repressing deleterious mutations andallowing for recombination); anisogamy was a laterdevelopment. However, as commonlyacknowledged (Williams, 1975; Maynard Smith,1978; Maynard Smith and Szathmáry, 1995), theevolution of sex is far from well understood. Aradical alternative to the classical model (Walther,2000) is original anisogamy through the fusion oftwo prokaryotic organisms in a predatorial/symbioticevent. This would mean that eukaryotic sex, likeeukaryotes themselves, is the result of predation.Does the fossil record have anything to sayabout this? Although the record is fundamentallyinadequate to illuminate processes at the level oforganelles, some important information about earlyeukaryote evolution is in fact available. Cavalier-Smith (1987a) proposed that the original bacterialsymbiotic host, in order to be capable of engulfingother organisms, must have lost its polysaccharidecell wall and compensated this by evolving aninternal cytoskeleton and sterol cell membranes.Sterols (a group of steroid lipids) are an importantand characteristic component of eukaryote cellmembranes. The degradation products ofeukaryotic sterols, C 27–C 29steranes, have beendiscovered in 2.7 billion-year-old organic mattertogether with 2-methylhopanes, a knowndegradation product of cyanobacterial membranelipids (Brocks et al., 1999; Summons et al., 1999).Thus there is fossil chemical evidence that by thattime at least two of the organismal groups thatparticipated in the symbiotic events leading up toeukaryotic cells were present in the biosphere.With regard to body fossils, the generally largersize of modern eukaryotic cells with respect toprokaryotic cells was used in a pioneering attemptto date eukaryote origins based on the sizedistribution of Precambrian microfossils (Schopfand Oehler, 1976). The earliest fossil nowcommonly attributed to eukaryotes is the 1.85billion-year-old (Hoffman, 1987; Morey and293