Evolutionary Neuroscience

923 Pages·2020·35.851 MB·English

by  Jon H. Kaas (editor)

EVOLUTIONARY
NEUROSCIENCE
SECOND EDITION
Edited by
Jon H Kaas
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Contributors
J.S.Albert UniversityofLouisiana,Lafayette,LA,United W.A.Freiwald NationalInstitutesofHealth,Bethesda,MD,
States UnitedStates;UniversityofRochester,Rochester,NY,
B.M.Arsznov Minnesota StateUniversity Mankato, UnitedStates;TheRockefellerUniversity,NewYork,NY,
UnitedStates
Mankato,MN,UnitedStates
K.W.S.Ashwell TheUniversityofNewSouthWales, A.B.Goldring UniversityofCalifornia,DavisCenterfor
Neuroscience,Davis,CA, UnitedStates
Sydney,NSW,Australia
A.M.Balanoff JohnsHopkinsUniversity,Baltimore,MD, A.Gonza´lez UniversityComplutense ofMadrid,Madrid,
Spain
UnitedStates;JohnsHopkinsUniversitySchoolof
Medicine,Baltimore,MD,UnitedStates O.Gu¨ntu¨rku¨n Ruhr-UniversityBochum,Bochum,Germany
M.K.L.Baldwin UniversityofCalifornia,Davis,Davis,CA, A.-M.Hartmann CarlvonOssietzkyUniversityOldenburg,
UnitedStates;MonashUniversity,Clayton,VIC,Australia Oldenburg,Germany
H.ClarkBarrett UCLA,LosAngeles,CA,UnitedStates S.Herculano-Houzel VanderbiltUniversity,Nashville,TN,
G.S.Bever JohnsHopkinsUniversity,Baltimore,MD, UnitedStates
UnitedStates;JohnsHopkinsUniversitySchoolof L.Z.Holland UniversityofCaliforniaatSanDiego,LaJolla,
Medicine,Baltimore,MD,UnitedStates CA,UnitedStates
O.R.P.Bininda-Emonds CarlvonOssietzkyUniversity J.H.Kaas Vanderbilt University,Nashville, TN,United
Oldenburg,Oldenburg,Germany States
C.Boeckx ICREA,UniversitatdeBarcelona,Barcelona, A.R.Kriegstein UniversityofCalifornia,SanFrancisco,San
Spain Francisco,CA,UnitedStates
B.Bogin LoughboroughUniversity,Loughborough,United F.M.Krienen HarvardMedicalSchool, Boston,MA,United
Kingdom States;BroadInstitute,Cambridge,MA,UnitedStates;
J.A.Bourne UniversityofCalifornia,Davis, Davis,CA, HarvardUniversity,Cambridge,MA,UnitedStates;
MassachusettsGeneralHospital,Boston,MA,UnitedStates
UnitedStates;MonashUniversity,Clayton,VIC,Australia
E.K.Boyle GeorgeWashingtonUniversity,Washington,DC, L.A.Krubitzer UniversityofCalifornia,DavisCenterfor
UnitedStates Neuroscience,Davis,CA, UnitedStates
A.Bringmann University ofLeipzig FacultyofMedicine, G.Laurent MaxPlanckInstituteforBrain Research,
Frankfurt,Hessen,Germany
Leipzig,Germany
E.Bruner CentroNacionaldeInvestigacio´nsobrela D.A.Leopold NationalInstitutes ofHealth,Bethesda, MD,
Evolucio´nHumana,Burgos,Spain UnitedStates;UniversityofRochester,Rochester,NY,
UnitedStates;TheRockefellerUniversity,NewYork,NY,
R.L.Buckner HarvardMedicalSchool, Boston,MA,United
UnitedStates
States;BroadInstitute,Cambridge,MA,UnitedStates;
J.M.Lo´pez University ComplutenseofMadrid,Madrid,
HarvardUniversity,Cambridge,MA,UnitedStates;
Spain
MassachusettsGeneralHospital,Boston,MA,UnitedStates
E.Candal UniversidadedeSantiagode Compostela, P.R.Manger University ofthe Witwatersrand,
SantiagodeCompostela,Spain Johannesburg,SouthAfrica
T.A.Chaplin MonashUniversity,Melbourne,VIC,Australia S.Mayer UniversityofCalifornia,SanFrancisco,San
Francisco,CA,UnitedStates
J.D.Cosman VanderbiltUniversity,Nashville,TN,United
M.Megı´as University ofVigo,Vigo,Spain
States;Queen’sUniversity,Kingston,ON,Canada;
Universite´PierreetMarieCurie,InstitutduCerveauetdela J.F.Mitchell National InstitutesofHealth,Bethesda,MD,
Moellee´pinie`re,Paris,France UnitedStates;UniversityofRochester,Rochester,NY,
B.L.Finlay Cornell University,Ithaca,NY,UnitedStates UnitedStates;TheRockefellerUniversity,NewYork,NY,
UnitedStates
J.G.Fleagle StonyBrookUniversity,StonyBrook,NY,
N.Moreno UniversityComplutense ofMadrid,Madrid,
UnitedStates
Spain
xi
xii
Contributors
R.Morona UniversityComplutense ofMadrid,Madrid, J.D.Schall VanderbiltUniversity,Nashville,TN,United
Spain States;Queen’sUniversity,Kingston,ON,Canada;
C.F.Moss JohnsHopkinsUniversity,Baltimore,MD,United Universite´PierreetMarieCurie,InstitutduCerveauetdela
States Moellee´pinie`re,Paris,France
R.K.Naumann MaxPlanckInstitutefor BrainResearch, M.S.Schall Vanderbilt University,Nashville, TN,United
States;Queen’sUniversity,Kingston,ON,Canada;
Frankfurt,Hessen,Germany
Universite´PierreetMarieCurie,InstitutduCerveauetdela
J.M.P.Pakan University ofEdinburgh,Edinburgh,United
Moellee´pinie`re,Paris,France
Kingdom
E.R.Seiffert UniversityofSouthernCalifornia,LosAngeles,
M.Pare´ VanderbiltUniversity,Nashville,TN,UnitedStates;
CA,UnitedStates
Queen’sUniversity,Kingston,ON,Canada;Universite´
M.Stacho Ruhr-UniversityBochum,Bochum,Germany
PierreetMarieCurie,InstitutduCerveauetdelaMoelle
e´pinie`re,Paris,France I.Stepniewska VanderbiltUniversity,Nashville,TN,United
M.A.Pombal UniversityofVigo,Vigo,Spain States
S.Pose-Me´ndez Universidadede SantiagodeCompostela, S.J.Sterbing-D’Angelo University ofMaryland,College
SantiagodeCompostela,Spain Park,MD,UnitedStates;JohnsHopkinsUniversity,
Baltimore,MD,UnitedStates
P.Pouget VanderbiltUniversity,Nashville,TN,United
G.F.Striedter UniversityofCalifornia,Irvine,CA, United
States;Queen’sUniversity,Kingston,ON,Canada;
Universite´PierreetMarieCurie,InstitutduCerveauetdela States
Moellee´pinie`re,Paris,France F.Stro¨ckens Ruhr-UniversityBochum,Bochum,Germany
T.M.Preuss EmoryUniversity,Atlanta,GA,UnitedStates R.Uchiyama CornellUniversity,Ithaca,NY,UnitedStates
H.-X.Qi VanderbiltUniversity,Nashville,TN,UnitedStates C.Varea UniversidadAuto´nomadeMadrid,Madrid,Spain
I.Quintana-Urzainqui Universidade deSantiagode S.P.Wise Olschefskie Instituteforthe Neurobiologyof
Compostela,SantiagodeCompostela,Spain Knowledge,Potomac,MD,UnitedStates
J.P.Rauschecker GeorgetownUniversity MedicalCenter, B.Wood GeorgeWashington University,Washington,DC,
Washington,DC,UnitedStates;TUM,Munich,Germany UnitedStates
A.Reichenbach UniversityofLeipzigFacultyofMedicine, DouglasWylie DepartmentofBiologicalSciences,
Leipzig,Germany UniversityofAlberta,Edmonton,AB,Canada
I.Rodrı´guez-Moldes Universidade deSantiagode KaraE.Yopak University ofNorth CarolinaWilmington,
Compostela,SantiagodeCompostela,Spain DepartmentofBiologyandMarineBiology,Wilmington,
M.G.P.Rosa MonashUniversity,Melbourne,VIC,Australia NC,United States
T.B.Rowe The UniversityofTexasat Austin,Austin,TX, H.-H.Yu MonashUniversity,Melbourne, VIC,Australia
UnitedStates W.Zinke VanderbiltUniversity,Nashville,TN,United
S.T.Sakai MichiganState University,EastLansing, MI, States;Queen’sUniversity,Kingston,ON,Canada;
UnitedStates Universite´PierreetMarieCurie,InstitutduCerveauetdela
Moellee´pinie`re,Paris,France
G.N.Santos-Dura´n Universidade deSantiagode
Compostela,SantiagodeCompostela,Spain
C H A P T E R
1
A History of Ideas in Evolutionary Neuroscience
G.F. Striedter
University of California, Irvine, CA, United States
Glossary
scrambles the chronology of theoretical developments
but helps to disentangle the diverse strands of thought
allometry Thenotionthatchangesinthesizeofanobject
that currently characterize evolutionary neuroscience.
(e.g.,thebodyorthebrain)entailpredictable
changesintheproportionalsizesofitscom- Italsohelpstoclarifywhichfuturedirectionsarelikely
ponents. In contrast, isometric scaling in- to bemostfruitfulfor thefield.
volvesnochangesinanobject’sproportions.
convergence Theindependentevolutionofsimilarstructures
orfunctionsfromnon-homologousancestral
1.1 Common Plan versus Diversity
precursors.
developmental Thenotionthatthemechanismsofdevelopment
constraint bias the production of phenotypic variants Oneofthemostfamousbattlesofideasincomparative
thatnaturalselectioncanacton.
biology was that between Etienne Geoffroy St. Hilaire
encephalization Brainsizerelativetowhatonewouldexpectin
and George Cuvier over the existence, or not, of a com-
an organism of the same type (i.e., species
or other taxonomic group) and body size. mon plan of construction (or Bauplan) for animals
Synonym:relativebrainsize. (Appel, 1987). Geoffroy was of the opinion, previously
heterochrony Phylogenetic changes in the relative timing of developedbyBuffon(1753),thatallanimalsarebuiltac-
developmentaleventsorintherelativerates
cordingtoasingleplanorarchetype,butCuvier,France’s
ofdevelopmentalprocesses.
most illustrious morphologist, recognized at least four
homology Therelationshipbetweentwoormorecharacters
that were continuously present since their differenttypes.Theirdisagreementeruptedintothepub-
origin in a shared ancestor. For a more licspherewhenGeoffroyin1830endorsedtheviewthat
detailed definition, especially for neural theventralnervecordofinvertebratesisdirectlycompa-
characters,seeStriedter(1999).
rable (today we say ‘homologous’) to the spinal cord of
mosaicevolution The notion that, as brains evolve, individual
vertebrates. Cuvier responded that Geoffroy was specu-
brain regions may change in size indepen-
dentlyofoneanother.Incontrast,concerted lating far beyond the available data, and he reasserted
evolution indicates that brain regions must publicly that the major types of animals could not be
changetheirsizeinconcertwithoneanother. linked by intermediate forms or topological transforma-
tions.ThisCuviereGeoffroydebatewasfollowedclosely
The field of evolutionary neuroscience is more than by comparative biologists all across Europe, who were
100 years old, and it has deep pre-evolutionary roots. already flirting with the idea of biological evolution or,
Because that illustrious history has been reviewed as they called it, the transmutation of species. If Cuvier
repeatedly (Northcutt, 2001; Striedter, 2005) and is was right, then evolution was impossible. On the other
treatedpiecemealinseveral articles ofthisbook,Ishall hand, some of Geoffroy’s hypotheses (e.g., his proposal
not review it fully. Instead, I will discuss a selection of that insect legs correspond to vertebrate ribs) did seem
the field’s historically most important ideas and how a trifle fanciful. Thus, the CuviereGeoffroy debate
they fit into the larger context of evolutionary theory. I embodied much of the ambivalence surrounding evolu-
also emphasize ideas that are, or were, controversial. tioninthefirsthalfofthenineteenthcentury.
Specifically,Ipresentthefield’scentralideasincontrast After Darwin offered a plausible mechanism for the
pairs,suchas‘commonplanversusdiversity’and‘nat- transmutationofspecies,namely,naturalselection(Dar-
ural selection versus constraints’. This approach win, 1859), the idea of biological evolution took hold
EvolutionaryNeuroscience,SecondEdition
https://doi.org/10.1016/B978-0-12-820584-6.00001-5 3 Copyright©2020ElsevierLtd.Allrightsreserved.
4
1. AHistoryofIdeasinEvolutionaryNeuroscience
and, by extension, Geoffroy’s ideas gained currency. opposite, namely, the notion that phylogeny creates
Innumerable homologies were sought and, frequently, ontogeny (see Gould, 1977). Haeckel also promoted the
revealed(Russel,1916).Mostimpressivewasthediscov- ideathatallvertebratespassthroughahighlyconserved
ery of extensive molecular homologies between species phylotypicstageofembryonicdevelopment(Slacketal.,
that span the metazoan family tree (Schmidt-Rhaesa, 1993).Studieshave,however,challengedthephylotypic
2003). It was striking, for example, to discover that stage idea by showing that the major groups of verte-
many of the genes critical for early brain development brates can be distinguished at all stages of embryogen-
are homologous between insects and vertebrates esis (Richardson et al., 1997). An intriguing aspect of
(Sprecher and Reichert, 2003). Indeed, the invertebrate thatearlyembryonicvariabilityisthatitconsistsmainly
and vertebrate genes are sometimes functionally inter- of differences in the timing of developmental processes
changeable (Halder et al., 1995; deRobertis and Sasai, (Richardson, 1999). Little is known about the genes
1996). Those discoveries supported Geoffroy’s view that generate those changes in developmental timing
that all animals were built according to a common (alsoknownasheterochrony),butsomeofthem,atleast,
plan, which could now be understood to be a common arelikelytobefairlywellconservedacrossspecies(Pas-
genetic blueprint or ‘program’ (Gehring, 1996). Indeed, quinelli and Ruvkun, 2002). More importantly, the
many biologists proceeded to search for molecular ge- notionthatadultdiversityisbasedonevolutionchang-
netic homologies that could reveal previously unima- ing the temporal relationships of conserved processes
gined morphological homologies (Janies and DeSalle, represents another reconciliation of Cuvier’s insistence
1999). Geoffroy would have been thrilled. There are, on adult diversity with Geoffroy’s belief in a common
however, problems with the view that animals are all plan. Thus, the field of evolutionary developmental
alike. biology (evo-devo for short) has overcome the once so
Themostseriousproblem,inmyview,isthathomol- prominent dichotomy between conservation and diver-
ogousgenesmaysometimesbeinvolvedinthedevelop- sity. Its major challenge now is to discover the mecha-
mentofadultstructuresthatareclearlynothomologous nistic details of how conserved genes and processes
(Striedter and Northcutt, 1991). For example, insect areable to producesuch diverseadult animals.
wings and vertebrate nervous systems both depend on Evo-devo thinking has also invaded neuroscience,
hedgehog function for normal development, but this but evo-devo neurobiology still emphasizes conserva-
does not make neural tubes and insect wings homolo- tionoverdiversity.Forexample,wenowhaveextensive
gous (Bagunea and Garcia-Fernandez, 2003). Instead, evidencethatallvertebratebrainsareamazinglysimilar
findings such as this suggest that evolution tends to atveryearlystagesofdevelopment(Puellesetal.,2000;
work with highly conserved ‘master genes’ (Gehring, Puelles and Rubenstein, 2003). However, we still know
1996) or, more accurately, tightly knit assemblies of very little about how and why brain development di-
crucial genes (Nilsson, 2004), which it occasionally re- verges in the various vertebrate groups after that early,
shuffles by altering their upstream regulatory elements highly conserved stage or period. Looking beyond ver-
and/or downstream targets. Evolution is a terrific tebrates,wefindthatinsectbraindevelopmentinvolves
tinkerer that manages to create novelty fromconserved at least some genes that are homologous to genes with
elements. This conclusion echoes Geoffroy’s arguments similar functions in vertebrates (Sprecher and Reichert,
insofar as it acknowledges that ‘‘Nature works 2003).Thisisremarkablebutdoesnotprovethatinsects
constantly with the same materials’’ (Geoffroy, 1807), andvertebratesarebuiltaccordingtoacommonplane
but it does not mesh with the view that evolution built ifbythatwemeanthatthevariouspartsofadultinsect
all animals according to a single plan. What we have, brainsallhavevertebratehomologues.Forexample,the
then,isatleastapartialrapprochementofthepositions finding that several conserved genes, notably Pax6, are
held by Cuvier and Geoffroy: adult organisms do critical to eye development in both invertebrates and
conform to several different body plans, but they are vertebrates,doesnotindicatethatallthoseeyesarebuilt
built by shuffling repeatedly a highly conserved set of according to a common plan. The crucial question,
genes (Raff, 1996). Therefore, a crucial question for which we are just beginning to explore, is how the
research is how evolutionary changes in networks of conserved genes are tinkered with (reshuffled, co-
developmentallyimportantgenesinfluenceadultstruc- opted, or redeployed) to produce very different adult
tureand function. eyes(Zuberetal.,2003;Nilsson,2004).This,then,seems
Implicitintheprecedingdiscussionhasbeentheidea to be the future of evo-devo neurobiology: to discover
that adult species differences arise because of evolu- how highly conserved developmental genes and pro-
tionary changes in development (Garstang, 1922). This cesses are used to different ends in different species.
idea is commonly accepted now, but, back in the nine- As I have discussed, this research program has ancient
teenthcentury,Haeckel(1889)usedtopromoteitspolar roots,but it isjust now becoming clear.
1.History,Concepts,andTheory
1.2 ScalaNaturaeVersusPhylogeneticBush 5
1.2 Scala Naturae versus Phylogenetic Bush 1936) fractionates into a multitude of different chains,
none of which hasany special claim to being true.
Theideaofevolutionproceedingalongsomekindof This multiple-chains idea becomes self-evident once
scale from simple to complex also has pre-evolutionary we have grasped that species phylogenies are just like
roots.Aristotle,forexample,orderedanimalsaccording human family trees; they are neither ladders, nor trees
to the degree of perfection of their eggs (see Gould, with just a single trunk, but bushes or tumbleweeds
1977). Later religious thinkers then described an elabo- (Striedter,2004)withbranchesgrowingindivergentdi-
ratescaleofnature,orscalanaturae,withinanimatema- rections. Within a given branch, or lineage, complexity
terialsonitsbottomrungandarchangelsandGodatthe may have increased at some points in time and
otherextreme.Theearlyevolutionists,suchasLamarck, decreased at others, but even if complexity increased
transformed this static concept of a scala naturae into a morefrequentlythanitdecreased,theover-allphylog-
dynamic phylogenetic scale that organisms ascended eny would fail to yield a single scale, because
as they evolved. Darwin himself had doubts about ar- complexitytendstoincreasedivergentlyindifferentlin-
ranging species on a scale, but most of his followers eages.Forexample,bats,honeybees,andhummingbirds
had no such qualms (Bowler, 1988). Even today, the are all incredibly complex, compared to their last com-
phylogeneticscaleistaughtinmanyschoolsanditper- mon ancestor, but they are each complex in different
sists in medicine and academia. For example, the Na- ways. Of course, we can pick one parameter and build
tional Institutes of Health’s (NIH) guide for ascaleforthatewecan,forinstance,comparetheabil-
institutional animal care and use still recommends that ityofbats,honeybees,andhummingbirdstoseeultravi-
researchers,wheneverpossible,shouldworkwith‘‘spe- olet (UV) radiation e but different parameters might
ciesloweronthephylogeneticscale’’(Pitts,2002,p.97). well yield different scales. Simply put, changes that
On the other hand, most contemporary evolutionists occurred divergently in different lineages will not, in
have pronounced as dead both the scala naturae and its general,produceasingleoverarchingscale.Thisinsight
postevolutionary cousin,the phylogenetic scale (Hodos is old hat to evolutionary biologists, but news to many
andCampbell,1969).Whatdothosemodernevolution- neuroscientists (Hodos and Campbell, 1969). In part,
ists cite as the scales’ causeofdeath? therefore, the persistence of scala naturae thinking in
Onefatalflawintheidea thatspeciesevolvealonga the neurosciences reflects a lack of proper training in
singlescaleisthat,aswenowknow,evolutionmadeat contemporaryevolutionarytheory.Inaddition,Isuspect
least some species simpler than their ancestors. Sala- that human minds possess a natural tendency for
manders, for example, are much simpler, especially in ordering disparate items linearly. Such a bias would be
brainanatomy(Rothetal.,1993),thanonewouldexpect useful in many contexts, but it would make it difficult
from their phylogenetic position. Even more dramati- to comprehend (without training) the divergent nature
cally, the simplest of all animals, the placozoans, are of phylogeny.
nowthoughttohaveevolvedfromfarmorecomplicated Although scala naturae thinking persists in neurosci-
ancestors (Collins, 1998). As more and more molecular ence generally, evolutionary neuroscientists have
dataareusedtoreconstructphylogenies,itisbecoming laboredtoexpungeitsghost.Forexample,aconsortium
apparentthatsuchsecondarysimplificationofentirean- of28comparativeneurobiologistsrevisedthenomencla-
imals has occurred far more frequently than scientists ture of avian brains to replace the terms neostriatum,
had previously believed (Jenner, 2004) e perhaps archistriatum, and paleostriatum e which suggested
because they were so enamored of the phylogenetic that brains evolved by the sequential addition of new
scale. A second major problem with scala naturae brainregionsewithtermsdevoidofscalanaturaeover-
thinkingisthattheorderofspecieswithinthescalede- tones(Reineretal.,2004a,2004b;Jarvisetal.,2005).Some
pends on which organismal features we consider. For of the replacement names are terms that were already
example,manyfisheswouldrankhigherthanmammals used for brain regions in other vertebrates; they reflect
if we based our scale on skull complexity, which was our current understanding of homologies. However,
reduceddramaticallyasearlymammalsevolved(Sidor, some ofthenew terms ee.g., nidipalliumandarcopal-
2001). Similarly, dolphins rank high if we look only at lium e are novel and intended to apply exclusively to
brain size, but relatively low if we consider neocortical birds. These novel names were coined because bird
complexity, which was reduced as the toothed whales brains, particularly bird forebrains, have diverged so
evolved(MorganeandJacobs,1972).Mostpeopletacitly muchfromthoseofothervertebrates(includingreptiles)
agree that ‘higher animals’ are warm-blooded, social, that strict one-to-one homologies are difficult, if not
curious, and generally like us, but once we try to be impossible, to draw for several regions (Striedter, 1998,
more objective, the single ‘chain of being’ (Lovejoy, 1999). Thus, the revised terminology reflects a new
1.History,Concepts,andTheory
6
1. AHistoryofIdeasinEvolutionaryNeuroscience
consensus view that avian brains did not evolve by the frequently discussed, justification for examining the
sequentialadditionofnewbrainareas,yetalsoreminds brains of diverse species is that comparative research
usthatbirdbrainsarefulloffeaturesthatevolvedquite can bring to light convergent similarities, which in
independentlyofthosethatfeatureinmammalianphy- turn might reveal some principles of brain design. For
logeny.Inotherwords,thenewterminologyavoidsscala example, the discovery that olfactory systems in both
naturaeovertonesand,instead,combinesthenotionofa vertebrates and many different invertebrates exhibit
common plan with that ofdivergent complexity. distinctive glomeruli strongly suggests that those
Ascomparativeneurobiologistsrejectthenotionofa glomeruli are needed for some critical aspects of
scala naturae, they stand to lose a central part of their odorant detection and analysis (Strausfeld and Hilde-
traditional justification for working on nonhuman brand, 1999).
brains.Nolongercantheyarguethatresearchonother Therefore,researchonnonhumanbrainsneednotbe
brainsmustbeusefulbecausenonhumanbrainsareal- justified in terms of a presumed phylogenetic scale.
wayssimpler,andthereforeeasiertocomprehend,than Instead, comparative neurobiology is valuable because
human brains. Instead, they must admit that some (1) all brains are likely to share some features, (2)
nonhuman brains are stunningly complex and, more nonhuman brains are more amenable to some types of
importantly, that their phylogenetic paths toward research,and(3)thestudyofdiversenonhumanbrains
complexity diverged from the primate trajectory. That canleadtothediscoveryofdesignrulesforbrains.His-
is,complexbird,fish,orinsectbrainsarenotmeresteps torically, only the first of these alternatives has been
along the path to human brains, but the outcome of widely discussed, but all are logically sound, and none
divergent phylogenies (see “Evolution of the Nervous dependon the existence of a scala naturae.
System in Fishes,” “Do Birds and Reptiles Possess Ho-
mologues of Mammalian Visual, Somatosensory, and
Motor Cortices?,” “Evolution of Color Vision and Vi- 1.3 Relative Size versus Absolute Size
sual Pigments in Invertebrates”). Does this suggest
that research on nonhuman brains should cease to be The most obvious difference between species is that
funded?Idonotthinkso,butthejustificationforwork- they differ enormously in size. Because life began with
ing on nonhuman brains ought to be tweaked. One tiny organisms, evolutionary increases in body size
obvious alternative justification is that all brains are must have outnumbered or outpaced the decreases.
likely to share some features, especially if they come This is true of organisms generally, but it also holds
from close relatives. Another good justification for for several individual lineages, including mammals
research on nonhuman brains is that, compared to hu- and, within mammals, primates (Stanley, 1973; Alroy,
man brains, the former are much more amenable to 1998). The most fascinating aspect of those changes in
physiological and anatomical research. This line of bodysizeisthattheyinvolvedmuchmorethantheiso-
justification assumes that the model differs from the metric scaling up or down of the ancestral condition;
target system only in those respects that make the they involved allometric changes in the proportions of
model easier to study, and not in the respects that are body parts and physiologic processes. For example,
modeled e an assumption that sometimes fails. It skeletal mass increases disproportionately with
now appears, for example, that the auditory system of increasing body size, whereas heart rate decreases.
owls, which was generally regarded as an ideal model Countless studies e on both vertebrates and inverte-
for sound localization in vertebrates, exhibits some brates e have documented these allometries and
highly specialized features (McAlpine and Grothe, explored their functional implications (Calder, 1984;
2003). This finding, at first glance, suggests that Schmidt-Nielsen,1984).
research on bird brains is wasteful, but this is a Much less is known about the causes of allometry.
simplisticview.Researchontheowl’sauditorysystem Studiesonallometryininsectsshowedthatsomescaling
has taught us much about how neurons compute relationships arereadily modifiableby natural or artifi-
behaviorally relevant information and it serves as an cial selection (see Emlen and Nijhout, 2000; Frankino
invaluable reference against which we can compare etal.,2005).Thisfindingsuggeststhateventightscaling
sound processing in other species, including humans. laws are not immutable, which would explain why
Furthermore, some differences between a model and many traits scale differently (e.g., with different expo-
its target can lead to surprising discoveries. Much nents)indifferenttaxonomicgroups(PagelandHarvey,
might be gained, for example, from studying why 1989).Averydifferent,moretheoreticallineofresearch
some nonhuman brains are far more capable than pri- hasshownthatnumerousallometries,specificallythose
mate brains of repairing themselves (Kirsche and Kir- with power law exponents that are multiples of 1/4,
sche, 1964). Thus, model systems research can be may have evolved because the optimal means of deliv-
useful even if the model is imprecise. A third, less ering metabolic energy to cells is through an
1.History,Concepts,andTheory
7
1.3 RelativeSizeVersusAbsoluteSize
hierarchically branching, fractal network of vessels Overall,suchphylogeneticanalysessuggestthat,among
whose termini (e.g., capillaries) are body size-invariant vertebrates, relative brain size increased more
(West et al., 1997; Savage et al., 2004; West and Brown, frequentlythan it decreased(Striedter,2005).
2005). This theory is mathematically complex and still Enormousefforthasgoneintodeterminingthefunc-
controversial (Kozlowski and Konarzewski, 2004; tional significance of evolutionary changes in braine
Brownetal., 2005; Hoppeler and Weibel, 2005),but it is bodyscaling.Darwin,forexample,hadarguedthatrela-
elegant. Furthermore, because the theory of West et al. tive brain size is related to ‘‘higher cognitive powers’’
isbasedinpartontheassumptionthatnaturalselection (Darwin, 1871), but defining those powers and
optimizes phenotypes, it is consistent with the afore- comparing them across species has proven difficult
mentionedfindingthatallometriesaremodifiablebyse- (Macphail,1982).Consequently,mostsubsequentinves-
lection. However, West et al.’s (1997) theory cannot tigators shied away from the notion of general intelli-
explain (or does not yet explain) why some organs, gence, or ‘biological intelligence’ (Jerison, 1973), and
suchasthebrain,scalewithexponentsthatarenotmul- focusedinsteadonmorespecificformsofhighercogni-
tiplesof1/4.Norcaniteasilyexplaintaxonomicdiffer- tion. Parker and Gibson (1977), for example, proposed
ences in scaling exponents. Thus, the causal e that a species’ degree of encephalization is related to
physiological and/or developmental e bases of allom- its capacity for extracting nutritious fruits and nuts
etry are coming into focus but remain, for now, from their protective shells. Several authors have
mysterious. stressedcorrelationsbetweenbrainsizeand‘socialintel-
Brain scaling, in particular, remains quite poorly un- ligence’(ByrneandWhiten,1988;Dunbar,1998;Reader
derstood (see “Principles of Brain Scaling,” “Scaling andLaland,2002).Collectively,thesestudiesreinforced
theBrainandItsConnections,”“HowtoBuildaBigger thesensethatrelativebrainsizeis,somehow,relatedto
Brain; Cellular Scaling Rules for Rodent Brains”). The someformsofintelligence.However,relativebrainsize
discovery that brains become proportionately smaller also correlates with several other attributes, such as
with increasing body size dates back to the late eigh- longevity, home-range size, diet, and metabolic rate
teenth century (Haller, 1762; Cuvier, 1805e1845). Since (for a review, see van Dongen, 1998). The lattercorrela-
then, numerous studies have documented brain allom- tions, with diet and metabolism, have received particu-
etry in all the major groups of vertebrates (Deacon, larly lavish attention (Martin, 1981; McNab, 1989;
1990a; van Dongen, 1998) and even some invertebrates Aiello and Wheeler, 1995). Paradoxically, the discovery
(JulianandGronenberg,2002;Maresetal.,2005).Gener- ofsomanycorrelationshasledsomeevolutionaryneu-
ally speaking, those studies confirmed that in double roscientists to despair: there are too many correlates of
logarithmic plots of brain size versus body size, the relative brain size, and many of them come and go,
data points for different species within a given lineage depending on which taxonomic group is being exam-
tendtoformareasonablystraightline,indicatingtheex- inedandwhichstatisticalmethodsareusedfortheana-
istenceofasimplepowerlaw.Theslopeofthosebest-fit lyses(e.g.,BennetandHarvey,1985;Iwaniuketal.,1999;
lines are almost always less than 1, which reflects the Deaner et al., 2000; Beauchamp and Ferna´ndez-Juricic,
aforementioned fact that brains generally become pro- 2004; Jones and MacLarnon, 2004; Martin et al., 2005).
portionately smaller with increasing body size. The Too manycontested hypotheses, too little certitude.
large body of work on brainebody scaling further Thereisalsonotmuchclarityonwhybrainsscaleso
revealedthatdatapointsfordifferenttaxonomicgroups predictably with body size. Early workers argued that
oftenformlineswithsimilarslopesbutdifferentyinter- brains generally scale against body size with a power
cepts.Thesedifferencesinyinterceptsareknownasdif- law exponent close to 2/3 because the brain’s sensory
ferences in relative brain size or encephalization. They and motor functions were related to the body’s surface
seriously complicate efforts to draw a single allometric area,whichpresumablyscaleswiththatsameexponent
line for any large taxonomic group (Pagel and Harvey, (Snell,1891;Jerison,1973).Accordingtothisview,brain
1989),buttheyallowustoidentifyevolutionarychanges sizes in excess of that predicted by the 2/3 power law
in relative brain size among some smaller taxonomic areduetoincreasesinthebrain’snonsomatic,cognitive
groups. For example, they allow us to determine that regions. This would explain the correlations between
relativebrainsizeincreasedwiththeoriginofmammals, relativebrainsizeandsomeformsofintelligence.Unfor-
with the origin of primates, several times within tunately, there are two major problems with this view.
primates, with the origin of the genus Homo, and, last First, brainebody scaling exponents often differ sub-
but not least, with the emergence of Homo sapiens stantially from 2/3 (van Dongen, 1998; Nealen and
(see“PrimateBrainEvolutioninPhylogeneticContext,” Ricklefs, 2001). The second problem is that the brain’s
“The Hominin Fossil Record and the Emergence of the more cognitive regions also scale predictably with
ModernHumanCentralNervousSystem,”“TheEvolu- body size (Fox and Wilczynski, 1986), undermining the
tion of Human Brain and Body Growth Patterns”). assumption that brains are divisible into regions that
1.History,Concepts,andTheory