~vo • utzon DOUGLAS J FUTUYMA State University of New York at Stony Brook Chapter 19, "Evolution of Genes and Genomes" by Scott V Edwnrds, Hnrvnrd University Chapter 20, "Evolution and Development" by foltn R Trlle, S/n/e UIl;versity of New York at Stony Brook SINAUER ASSOCIATES, INC • Publishers Sunderland, Massachusetts U.S.A Front cover Back cover The luxurious plumes of a male bird of pBradise (PnmdisnE'R rngginnn) ,'Ire the result of sexual selection (see Chapters 11 and 17) Photograph © Art \'Volfe/ Art Wolfe, Inc Modern birds are almost certainly descended from feathered dinosaurs, such as the famolls fossil Archaeopteryx litltogmphict1 Long flight feathers were borne by clawed hands and a long tail, characteristic of theropod dinosaurs but not of modern birds (see Chapter 4) Photograph © Tom Stack! Painet, Inc Evolution Copyright © 2003 by Sinauer Associates, Inc AU rights reserved This book may not be reprinted in ''''hole or in part ,,,,,ithout permission from the publisher: Sinauer Associates, Inc., 23 Plumtree Road, Sunderland, MA 01375 U.s.A FAX: 413-549-1118 W\'\"N.si nauer.com Sources of the scientists' photographs appearing ill Chapter are gr- :2 Au bahrelgllazaJi All (jllaIllCIISIS Kell)'all/hroplIs p/Clt)'OPS 'I Đ '-< I ~ H erectl/s • H ergaster , ' A II mrlolfemls ' I Paratlthropus Arl5lra}opirliccus bOiSCl !JnbiliS P robllstll~ • arl, .A, I /g "l: , ~ aerhiopicHS iI iii All afncallus ArdipilllCClI5 All afarcllSis ramidlls.l _ Ar kat/abba Figure 4.13 The approximate temporal extent of named hominin taxa in the fossil record The time span indicCltes either the range of dated fossils or the range of estimated dates for taxa known from few specimens (After Wood 2002.) _ _ _ _ Large brain, small teeth, obligate bipedalism Small brain, very large reeth, fucultative bipedalism Small brain, large teeth, facultative bipedalism Insufficient evidence SalrelalllhropHs tchadcllsis II T Orrorin tugCllClISis EVOLUTION IN THE FOSSIL RECORD 81 print traces have been found in rock formed from volcanic ash near an nfnrellsis site in Tanzania Following afarellsis in the late Pliocene and early Pleistocene, the number of hominin species and the relationships among them have not yet been resolved (Figure 4.13) Most authorities agree that hominin species were quite diverse at this time A lineage of "robust" australopithecines (ParnIlIIJropIlS), of which (A) Chimpanzee three species have been named, had large molars and premo- lars and other features adapted for powerful chewing; they probably fed on tubers and hard plant material The robust australopithecines may have made stone tools, the oldest of which are 2.6-2.3 Myr old However, they became extinct without hav- (B) AU5tmiopit/lCCllS afaremjs (3.5 M}'a) ing contributed to tl,e ancestry of modem hlunans A more slender form was AllstrnlopitIJeClls africoll1l5, which is generally tllOught to have descended from A afarellsis, but had a greater cranial capacity (about 450 cc), indicating a larger brain (Figure -l.14B,C) Some of the derived characters of afrieO/llls resemble those of robust australopithecines, so it may not be in the line of direct ancestry of modern humans The earliest fossils that are usually assigned to the genus HOlllo range from about 1.9 to 1.5 Mya (late Pliocene and early Pleistocene) Originally called HOlllo Iwbilis, they are variable enough to be assigned by some authors to two or even three species, H IJauilis, H ergasler, and H rlldolfensis HOIiIO Iwbilis (in the broad sense) is the epitome of a rediscovered missing link (Figme 4.140), a nd might better be assigned to A IIslm/opilIJeells (Wood and Collard 1999) The oldest specimens are very simiJar to AlIsfrnlopiflIeclIs nfricanus, and tlle YOlUlger ones grade into the later form HOlllo ereeills Compared with AlIslrn!opiIIJeells, Homo hnbiJis more nearly resembles modern humans in its greater cranial capacity (610 to nearly 800 cc), flatter face, and shorter tooth row Although the limbs retain apelike proportions that suggest an ability to climb, tl,e structure of tl,e leg and foot indicates that its bipedal locomotion was more nearly human than that of the austraJopithec.ines Homo hnbilis is associated with stone tools (referred to as Olduwan tecllllology) and with animal bones that bear cut marks and other signs of hominin activity (Potts 1988) Later hominin fossils, from about 1.6 Mya to about 200,000 years ago (200 Kya), are referred to HOlllo ereeills Most authorities think that lzabiJis, erectlls, and sapiens are a single evolutionary lineage In most respects, erect liS from the middle Pleis- (C) Allstralopitliews nfricmllls (3.0-2.5 i"l)'a) (D) Homo 1mbilis (1.9-1.5 Jo,,1ya) (El Homo crcct/lS (1.6-0.2 Mya) Fossil skulls of A ofarensis have characteristics similar to those of modern chimpanzees Over time, hominins evolved smaller canine teeth the opening for the spinal cord shifted forward tocene onward has fairly modem human features in its skull, in its postcranial anatomy, and in indications of its behavior The Figure 4.14 Frontal and lateral reconstructions of the skulls of a chimpanzee and some fossil hominins (A) Pall troglodytes, the chimpanzee Note large canine teeth, low forehead, prominent face, and brov.' ridge (B) Al/stralopitheclIs afarellsis Some of the same fea~ tures as in the chimpanzee arc evident (C) Austm/opiff/eells africanlls has smaller canines and a higher forehead (D) Homo lIabilis The face projects less, and the skull 15 more rounded, than in earlier forms (E) HOlllo ereetlls Note the still more vertical face and rounded forehead (F) Homo (sapiens) neandertlinlel/sis The rear of the skull is more rounded than in H erectlls, and cranial capacity is greater (A, B after Jones et al 1992; C-F after Howell 1978.) (F) Homo jnpicllj /lcmulerthalcl/sis (120-30 Kra) the face became more vertical (jaw less projected) and cranial capacity increased greatly 82 CHAPTER skull is rounded, the face is less projected than in earUer forms, the teeth are smaller, and the cranial capacity is larger, averagLng about 1000 cc and evidently increasing over time (Figure 4.14E) At least Mya (perhaps as far back as 1.7 Mya), ereetHs spread from Africa into Asia, extending eastward to China and Java TluDUghoLit its range, erectlls is associated witb stone tools, termed the Acheulian culture, that are nlDr€ diverse and sophisticated than the Olduwan tools of H Iwbilis The use of fire was widespread by hall a million years ago Homo erect1l5 grades into forms that have generally been ca1.led "archaic Homo sapiens," starting about 400 or 300 Kya During the history of sapiells, mean cranial capacity increased, from abou t 1175 cc at 200 Kyo to its modern mean of 1400 cc "Archaic sapiens" from the middle Pleistocene differs in relatively minor respects from the "anatomically modern sapiells" that appeared in the late Pleistocene The best-known populations of archaic Homo sapiens are the Neanderthals of Europe and south\vestern Asia, distinguished by some authors as a species, Homo Jlennderthnlensis Neanderthals had dense bones, thick skulls, and projecting brows (Figure 4.14F); contrary to the popular image of a stooping brute, Neanderthals walked fully erect, had brains as large as or even larger than ours (up to 1500 cc), had a fairly elaborate culture that included a variety of stone tools (Mousterian culture), and probably practiced ritualized burial of the dead Their remains extend from about 120 to 30 Kya "Modern sapiel/s," anatomically virtually indistiJlguishable from today's hUInans, appeared earlier in Africa (ca, 170 Kya) than elsewhere Modern humans overlapped with Neanderthals in ~le Middle East for much of the Neanderthals' history, but abruptly replaced them in Europe about 40,000 years ago As we shall see in Chapter 6, there is evidence that modern snpiens may have replaced archaic sapiens (including lIeallderthnlel1sis) without interbreeding-that is, the tvvo lineages may have been distinct biological species By 12,000 years ago, and possibly earlier, modern hwnans had spread from northeastern Asia across the Bering Land Bridge to northwestern North America, and thence rapidly throughout the Americas "Upper Paleolithic" culture emerged about 40 Kya The earliest of several successive cultural "styles" in EUJope, the AUl'ignacian, is marked by stone tools more varied and sophistkated thaJl those of the M.ousterian culnae Moreovel~ culture became ll10re than simply utilitarian: art, self-adornment, and possible mythical or religious beliefs are increasingly evident from about 35 Kya onward, Agriculture, which resulted in an enorlTIously increased human population density and began the human transformation of the Earth, is about 11,000 years old There is, at least at present, no way of knowing which (if any) of these cultural advances were associated with genetic changes in the capacity for reason, imagination, and awareness, but they are not paraUeled by any increase in brain size or other anatom ical changes, Throughout hominin evolution, different hominin features evolved at different rates ("mosaic" evolution) On average, brain size (cranial capacity) increased throughout hom.i.nin history, although not at a constant rate, and there were progressive changes, from afnrer/sis to africallll.s to ercctllS to sapiens, in many other features, such as the teeth, face, pelvis, bands, and feet The very fuzziness of the taxonomjc distinctions among the nalned forms attests to the mosaic and gradual evolution of hominin features Although many issues remain unresolved, the most i.l11portant point is fuJly documented: modem humans evolved h'om an apelike ancestor Why these d1anges occurred-what advantages they may have provided-is the subject of much speculation but only slight evidence (Lovejoy 1981; Fecligan 1986) What evidence exists is indirect, consisting mostly of inferences from studies of other primates, contemporary cultures, and anatomy and artifacts, The erect posture and bipedal locomotion are the first major documented changes toward tbe human condition A plausible hypotbesis is that bipedalism freed the arms for carrying food back to the social unit, especially to an individual's mate and offspring, Food sharing occurs i.n chimpanzees, which have a complex social structure that includes matrilocal family groups and "friendships." Chimpanzees also make and use a variety of simple tools, such as stone and wooden hammers they use to crack nuts, and twigs fash- EVOLUTION IN THE FOSSIL RECORD ioned to "fish" termites out of their nests The advantages gained by using a greater variety of tools may have selected for greater i.ntelligence and brain size Hov"evcr, many authors, beginning with Darwin, have emphasized that social interactions, such as learning how to provide parental care, forming cooperative liaisons with other group Inembers, detecting cheaters in social exchanges, and competing for resources within and among groups, 'would place a selective premium on intelligence, learning, and communication-thus selecting for greater i.ntelligence and a larger brain Dorsal 83 Ventral Phylogeny and the Fossil Record 1n inferring phylogenetic relationships alllong living taxa, we conclude that certai.n taxa share more recent C0l1Ull011 ancestors than others If SUdl statements are correct, then there should be some correspondence behveen the relative times of origin of taxa, as inferred from phylogenetic analYSiS, and their relative times of appearance in the fossil record \Ne can expect this correspondence to be imperfect becouse of the great imperfection of the fossil record; for example, a group that originated in the distant past might be recovered only from recent deposits Moreover, although a lineage may have branched off early, it may not have acquired its diagnostic characters until much later TIle synapsid clade, for example, did not acquire the diagnostic characters of mammals until long after it had diverged from other reptiles Nevertheless, there is a strong overall correspondence between phylogenetic branching order and order of appearance in the fossil record Just by phylogenetic analysis of living species, we i.nfer that the common ancestors of the different orders of mammals, of mammals and "reptiles," of these groups and amphibians, and of all tetrapods and sarcopterygian fishes are sequentially older The sequence in which tllese groups appear ill the fossil record matches the phylogeny A striking instance of correspondence is offered by the bristletaUs (order Archaeognatha), wingless insects that have long been thought to represent the basic "body plan" of ancestral insects (Figure 4.15) Recently, a fossil bristletail was discovered in early Devonian depOSits It is the oldest kno\ovn fossil insect, and it is as old as would be expected given the assumption that bristletails are phylogenetically more basal than the other insect orders Phylogenetic relationships can often be clarified by information from extinct species (Donoghue et al 1989) Some characters may have been so highly modified that it is difficult to trace their evolutionary transformations, or even to determine their homology Fossils may provide the cniCial missing uifonnation For example, some authors had postulated that mammals and birds are sister taxa, but the fossil record of mammal-like reptiles and dinosaur-like birds showed tilat this hypothesis \-vas wrong Evolutionary Trends The fossil record presents many instances of evoJutionary trends Among menlbers of tile horse family (Equidaet for example, average body size increased steadily over the course of almost 50 Myr (Figure 4.16A) Conunonly, some lineages buck the overall trend and undergo reversal, as is the case with body size in some equid lineages (Figure 4.16B) Certain evolutionary changes appear never to have been reversed, however Ever since 1\101'galll/codolJ, for example, manlmals have had a single lower jaw bone and have never reverted to the multiple bones of their ancestors Although we may have evidence that an evoJutionary change has never been reversed, we cannot be su.re that reversal is impossible 50lne feahaes may never have reverted sjmply because they are advantageous, or even necessary For example, even flightless birds such as ostriches and penguins have feathers because feathers provide insulation and are used in sexual and social displays Tn most vertebrates, the notocbord degenerates after its expression in early €lnbryonic development, but it is retained in the embryo because it induces the development of the central nervous system Rupert Riedl (1978) suggested that such a character carries a BUIWEN meaning a suite of other features that depend on it for their development or proper function It is, of course, possible that some changes are j A living bristletail (order Archaeognatha) Among extant orders of insects, bristletails have the most primitive features, such as the vestigial legs on the ventral surface of the abdominal segments, derived from the walking legs of ancestral arthropods Figure 4.15 (After CSIRO 1991.) 84 CHAPTER CAl -/'r £1""' ~, • (grazer) 'tr 400 • 350 450 co 0- 300 250 ~ II ~ ~ j • ~ 200 'S •• r:\ • •• 150 r {C~(:" : r) • •• cgra,W (browser) : I SOD '< Hyracotllerillll7 (browser) Mesohipplis • 550 • Mer)'chipPlIs • 100 SO (Bl 0.30 • • Size increase • Size decrease 0.26 • 0.22 '"~ "- g- o- Rate of body size evolution increased as horses shifted from forested environments to open grasslands • •• • • • • • • • • • • • 60 55 50 45 40 35 30 25 20 Time (~·Iya) IS • ~ ~ 0.14 < 2S o· 0.10 • • • 0.18 -;; ;:::; • •• • Evolution of body mass in the horse family, Equidae (A) EstilT'Iated body masses of 40 species, plotted against geological time Although SOlTte small species occurred throughout the history of the family, the average body size increased over time (B) Rate and direction of evolution of body mass between various pairs of ancestral and descendant equids, plotted against the midpoint between their geological ages Most lineages increased in mass (colored circles), but some decreased (black circles) (After MacFadden ·1986.) Figure 4.16 -"""", 0.06 " ~ :s truly irreversible, perhaps because the developrnental foundations of some characters have been lost in evolution [n general, it seems likely that complex characters, once lost, are not regained-a principle ca]led Dollo's law Many taxa in the fossil record display parallel trends For example, the horse family is only one of many animal clades in which average body size has increased-a generalization called Cope's rule lVfultiple lineages often evolve through similar stages, called grades For exan1pIe, balanomorph barnacles, which first appeared in the Cretaceous, are enclosed by a cone-shaped skeleton made up of a number of slightly overlapping plates Ancestrally, there were eight plates, but as the balanomorphs diversified in the Cenozoic, the proportion of genera with eight plates steadily declined, and the proportlon with fewer plates increased Several lineages independently evolved U1rough six-plate, fourplate, and even one-plate grades (Figure 4.17) Shells with fewer plates, and hence fewer lines of vulnerability between them, may provide greater protection against predatory snails (Palmer 1982) 0;: s Punctuated Equilibria Although we have described paleontological examples of gradual transitLons through intermediate states, these kinds of transitions are by no 10 S Present means universally found in the fossil record Lntermediate stages in the evolution of many higher taxa are not known, and many closely related species in the fossil record are separated by smaller but nonetheless distinct gaps Most paleontologists have followed Darwin in ascribing these gaps to the great incompleteness of tbe fossil record In 1972, Niles Eldredge and Stephen Jay Gould proposed a more complicated, and much more controversial, explanation, which they called punctuated equilibria Their hypothesis applies to the abrupt appearance of closely related species, not to higher taxa "PLlIlctuated equilibria" refers to both a pattern of cbange in the fossil record and a hypothesis about evolutionary processes A conunon pattern, Eldredge and Gould said, is one of long periods in which species exhjb,t little or no detectable phenotypic cbange, interrupted by rapid shifts from one such "equilibrium" state to another; that is, stasis that is "punctuated" by rapid change (Figure 4.18A) They contrasted this pattern with what they called phyletic gradualism, the tradibonal notion of slow, incremental change (Figure 4.186) The fossil record offers examples of both gradual and pLmcluated patterns A particularly well-documented instance of phyletic gradualism has beend~r;~ forcllanges in the molar teeth of a Lineage of grass-feeding voles (Aifilllomys occitnnl/s) in the late Pliocene and Pleistocene (Figure 4.19) Several molar characters of these rodents changed directionally throughout Europe, indicating that gene flow among populations enabled the entire species to respond as a "vhole to selection for i.ncreased tooth height (Chaline and Laurin 1986) In contrast, Metmmbdotos, a Miocene genus of ectoprocts (also known as bryozoans, or "moss animals"), clearly shows a pattern of punctuated equilibria (Fig0.02 85 EVOLUTION IN THE FOSSIL RECORD 1 111 ~,Jl • I~ • •• • Pyrgo1lln lIIi/fepome (1 plnte) ~thYlnSlllnlid", • • Tetradifa radin/a (4 plntes) • T et rael itidae I , Bn/nllIlS Cht!WlJ}n!IIS hnlrllloides illfer/exflls (6 plates) Ar~hacobalanidae co~on~ Detoll/cris brulllrea (8 plates) Chlhamaloidc,l A parallel trend The phylogeny of balanol1lorph barnacles shmvs the reduction in the number of shell plates that occurred during the Cenozoic in several independent lineages (see Figure 3.5) TIle verticnl axis is Hot lillie, bllt grade of orgallizatioll (pln/e f1l/lIIber), The drm-vings are from an extensive monograph on bamacles by Charles Darwin (After Palmer ]982; drawings by G Sowerby, from Darwin 1854.) Balanoidea Coronuloidea Figure 4.17 (8) Phyletic gr8dualisl1l (A) Hypotht'lical d.lIa ••• ' '.' , In the traditional model, evolutionary change is gradual and not necessarily associated with speciation • '., • • • Char::lcter value (e.g., size) Character value (C) Punctuated equilibrium Three models of evolution, as applied to a hypothetical set of fossils (A) 1~lypothetical values for a character in fossils recorded from different time periods These data might correspond to any of the models shmvn i.n panels B-D (8) The traditional "phyletic gradualism" model (C) The "punctuated equilibrium" model of Eldredge and Gould, in which morphological change ocell 1'5 in new species Morphological evolution, although rapid, is still gradual as shown in the inset (0) The "punctuated gradualism" model of Malmgren ct nl (1983) Figure 4.18 (D) Punctuated gradualism A lineage evolves in rapid spurts from one equilibrium to another, but speciation does not necessarily occur A daughter species diverges rapidly, then continues without further change " E i= Character vallie Character value Even rapid evolution is gradual, involving shifts in the mean value of a morphological character 86 CHAPTER Phyletic gradualism: change in a molar of the grassfeeding vole lvlimoll1ys Grass wears dmvn the molar surface, so it is advantageolls to have a high tooth with enamel (pink) and cement (brown) forming grinding ridges at the tooth's surface An index of Ch