Survival and Selection Biases in Early Animal Evolution and a Source of Systematic Overestimation in Molecular Clocks
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Survival and selection biases in early animal evolution and a source of systematic overestimation in molecular clocks Graham E. Budd1 and Richard P. Mann2;3 1 Dept of Earth Sciences, Palaeobiology, Uppsala University, Villavägen 16, Uppsala, Sweden, SE 752 36. [email protected] 2Department of Statistics, School of Mathematics, University of Leeds, Leeds LS2 9JT, United Kingdom. [email protected] 3The Alan Turing Institute, London NW1 2DB, United Kingdom 1 Abstract 2 Important evolutionary events such as the Cambrian Explosion have inspired many 3 attempts at explanation: why do they happen when they do? What shapes them, 4 and why do they eventually come to an end? However, much less attention has 5 been paid to the idea of a “null hypothesis” – that certain features of such diver- 6 sifications arise simply through their statistical structure. Looking back from our 7 own perspective to the origins of large groups such as the arthropods, or even the 8 animals themselves, will expose features that look causal but are in fact inevitable. 9 Here we review these features with particular regard to the Cambrian explosion. We 10 conclude that the fossil record of the late Ediacaran to Cambrian is very likely to 11 be recording a true evolutionary radiation at this time; and show how the unusually 12 rapid nature of this event leads to characteristic over-estimation of its time of origin 13 by molecular clock methods - an artefact that is likely to apply to other unusually 14 fast radiations too. 15 16 Keywords: Crown groups, diversification rates, the push of the past, molecular 17 clocks, Cambrian explosion. 1 18 Introduction 19 The early evolution of the animals remains a remarkably contentious topic, with a lack 20 of agreement even on fundamental issues such as when it took place. The majority view 21 in the field is probably that animals evolved considerably before their undoubted fossil 22 record commenced (e.g. [1][2][3][4][5]). Such a view is based on several lines of evidence: 23 (1) molecular dates, that have consistently placed the timing of (for example) bilaterian 24 origins tens to hundreds of millions of years before the Cambrian [2][4]; (2) biomarkers 25 that have been used to place the origin of sponges in the Cryogenian [6]; (3) a general 26 view about timing involving a necessary period of evolution being required before the 27 fossil record (and its biogeography) can be generated [7][8]; and (4) a view that the fossil 28 record is in general patchy and unlikely to be reliable in any useful way for documenting 29 the precise timing of animal origins (see discussion in [5]). 30 Standing against this sort of view is what is probably the minority one that the fossil 31 record of early animals can be read more or less “as is”, despite its obvious imperfections 32 [9][10][11][12]. In particular, the origin of bilaterian-like trace fossils from later than 560 33 Ma in the late Ediacaran [13] is seen as an important marker that provides a backstop 34 for the latest time of origin of crown-group bilaterians, and which probably indicates the 35 time of entry of stem-group bilaterians into the fossil record. The rapid, but resolvable, 36 appearance of body and trace fossil taxa in the succeeding Terreneuvian Series is thus 37 seen as the unfolding of the crown group bilaterian radiation. 38 It seems remarkable, on the face of it, that so well a documented phenomenon as the 39 Cambrian explosion can be open to such divergent interpretations. One reason why this 40 might be the case is that the basic “ground rules” are different in each sort of view. In 41 particular, there is an ancient tradition of viewing the animal phyla as being distinct 42 entities that cannot be easily compared to each other. Thus, it has become quite com- 43 monplace to argue that their morphological origins are essentially independent from each 44 other. Whilst such a view has been articulated in various ways by many people, one 2 Figure 1: A classical image of the parallel emergence of the phyla around the time of the early Cambrian from relatively simple (and thus unfossilisable) ancestors. Reprinted with permission from Bergström (1989) [14]. 45 classical image is the striking one of Bergström 1989 (Fig.1; [14]) that shows a series 46 of phyla emerging from a small, slug-like organism (a “procoelomate”) during a “forma- 47 tive interval” (c.f. Valentine’s “roundish flatworm” [15] and the "small, thin" ancestors 48 of Sperling and Stockey [4]). A more extreme version of such ideas is that the earliest 49 bilaterians closely resembled the planktonic larvae of the extant clades (e.g. [16], drawing 50 on the tradition that can be ultimately traced to Haeckel [17]). Buttressed by various 51 geological and developmental arguments, this hypothesis posits that such small, and by 52 their very nature hard-to-preserve tiny animals are meant to persist up many, if not all 53 stem groups that lead to the modern-day crown-group phyla. Hence, the appearance of 54 undoubted bilaterian fossils represents in each case the transition from the unfossilisable 55 proto-phylum member to a full-blown fossilisable taxon. Such a transition could be trig- 56 gered either by an environmental stimulus (typically oxygen levels rising) or presumably 57 by some necessary level of ecological complexity being reached. 58 It is surprisingly difficult to unpack the entire set of assumptions and traditions that 59 lie behind the first of these views, but some features stand out and can be critically 3 60 examined. The first is the assumption that for all or at least many bilaterian clades, 61 the ancestral state was a small body size which would be difficult to record in the fossil 62 record [18]. Small organisms often lack key features such as complex musculature, body 63 cavities and appendages, and it seems that the critical body length for these purposes is 64 around 1 mm (see discussion in [11]). Many living protostomes are indeed tiny, and some 65 phylogenetic reconstructions have suggested this is ancestral for the clade as a whole [19]. 66 Without a reliable and fully-resolved protostome phylogeny, such a view is difficult to 67 assess. Nevertheless, in recent years some relatively large Cambrian members of clades 68 that today consist of meiofaunal organisms have been discovered. Of course, simply 69 finding a single large member of a clade is not equivalent to demonstrating that large body 70 size is the ancestral state, but it does (considerably) weaken the assumption that small 71 body size must be, especially given evidence that old fossils preserve more plesiomorphic 72 character states than recent taxa do (having had less time to shed them; [20]). Another 73 point of dispute has been the placement of the “Xenacoelomorpha”, a clade that consists 74 of Xenoturbella and acoel and nematodermatid flatworms; different analyses have placed 75 them either as the sister group to all other bilaterians [21][22], or as sister group to the 76 Ambulacraria (echinoderms and hemichordates) [23]. It should be stressed, however, that 77 even if such a clade is the sister group to all other bilaterians, it does not immediately 78 follow that its simple morphology must represent the ancestral condition for bilaterians as 79 a whole (as in [21]). Determining this would require detailed character reconstruction at 80 the base of the rest of the bilaterians, which is currently a matter of considerable dispute, 81 and reference to the cnidarian outgroup. In order to present more crisp hypotheses, we 82 shall briefly examine the current evidence for various clades: 83 Annelids, phoronids, sipunculans, brachiopods, molluscs 84 This, the classical “Lophotrochozoa” grouping, may also include entoprocts, bryozoans 85 and nemerteans (for a recent discussion of all of the lophotrochozoans in their broadest 86 sense, see [24]). Most of the included clades have tiny members (e.g. the so-called 4 87 ‘archiannelids’ [25], Gwynia capsula [26] etc) but a secondary derivation of these seems 88 most likely (see e.g. [27][28] for annelids). In general, the lively debate around the origins 89 of this group includes the distinct possibility that fossilisable morphological features such 90 as sclerites and setae are plesiomorphic within them [10][29][30][31]. 91 Other spiralians 92 Other protostomes (excluding the ecdysozoans - see below) include the Gnathifera (gnathos- 93 tomulids, rotifers, micrognathozoans, and, it seems, chaetognaths [32]), and the “Roupho- 94 zoa” [33] consisting of platyhelminths and gastrotrichs; these two clades together may 95 be paraphyletic and give rise to the lophotrochozoans (see e.g. the summary of re- 96 cent progress in [34]). Such a reconstruction has been considered to suggest a primitive 97 small body size for the protostomes as a whole [19][33]. In particular, it has been 98 argued [33] that the coelomate condition in the spiralians is confined to the lophotro- 99 chozoans (i.e. annelids, brachiopods, molluscs etc) and arose from within a clade of 100 acoelomate, flatworm-like animals. Once again though, some recent molecular and fossil 101 discoveries have suggested the situation is not so simple. The inclusion of the relatively 102 large, and potentially fossilisable and coelomate chaetognaths within or as sister group of 103 the Gnathifera throws into question the primitive state in this clade ( [35]; c.f. [32][36]); 104 and even in the Rouphozoa, recent suggestions of large (> 10 cm) gastrotrichs in the 105 Cambrian [37] must bring the primitive character state in this clade under question as 106 well.