Apologetics – Catholic Beliefs submitted by Pat - CatholicMom.com

13 Pages·2010·0.31 MB·English

by  Lisa Hendey

http://informahealthcare.com/ahb
ISSN:0301-4460(print),1464-5033(electronic)
AnnHumBiol,2014;41(4):368–380
!2014InformaUKLtd.DOI:10.3109/03014460.2014.923938
REVIEW
Humans are not cooperative breeders but practice biocultural
reproduction
Barry Bogin1, Jared Bragg2, and Christopher Kuzawa2
1SchoolofSport,Exercise&HealthSciences,LoughboroughUniversity,Loughborough,UKand2DepartmentofAnthropology,Northwestern
University,Evanston,IL,USA
Abstract Keywords
14 Context: Alloparental care and feeding of young is often called ‘‘cooperative breeding’’ and Alloparenting,humanlifehistory,childhood,
16/ humansareincreasinglydescribedasbeingacooperativebreedingspecies. lifetimereproductiveeffort,longevity
6/ Objective:Tocriticallyevaluatewhetherthehumanoffspringcaresystemisbestgroupedwith
0
n thatofothercooperativebreeders.
o History
6 Methods: (1) Review of the human system of offspring care in the light of definitions of
3.7 cooperative,communalandsocialbreeding;(2)re-analysisofhumanlifetimereproductiveeffort. ReceivedMarch2014
220.23 Ralelosuplatsr:enHtualmbaenharveiporuordiuscdtieofnineadndcuoltfufsrpalrliyngratchaerrethaaren bdyistginecntetfircomkinsohtihperalospneec.iTehsisbseycsatuesme APuccbelipshteedd9onMlianye210614June2014
98. allowslocalflexibilityinprovisioningstrategiesandensuresthatcareandresourcesoftenflow
by between unrelated individuals. This review proposes the term ‘‘biocultural reproduction’’ to
m describethisuniquehumanreproductivesystem.Inare-analysisofhumanlifehistorydata,itis
e.conly. estimated that the intense alloparenting typical of human societies lowers the lifetime
care o reproductive effort of individual women by 14–29% compared to expectations based upon
healthnal us oCtohnecrlumsioamn:mHaulsm.ans are not cooperative breeders as classically defined; one effect of the
ao
ormpers urenpiqroudeucsttivraeteegffyorto,fwhhiucmhacnoulbdiohceulpltuerxapllarienplriofedsupcatnioenxteisnsaionl.owering of human lifetime
m infFor
o
d fr Introduction toanincreasedrateofreproductionand(4)decreasedlifetime
e
d reproductive effort, which likely contributed to decreased
oa Comparedwithmostspeciesofprimates,especiallytheapes,
nl mortality and lifespan extension.
w humans have an unusual style of producing and raising
o
D offspring that is often described as cooperative breeding
ol Cooperative breeding vs human cooperation in
Bi (Burkartetal.,2009;Hrdy,1999,2009).Thisspecialissueof reproduction
m the Annals of Human Biology focuses on ‘‘Human Biology
u
n H of the Past’’ and the evolution of the human biocultural style We begin by making our case for the introduction of the
An of reproduction is a central feature of the topic. Here we neologism biocultural reproduction, as distinct from recent
review evidence and provide new analyses showing that, workthatgroupsthetypeofhighlysocialchildcarepracticed
althoughsharingmanyfeatureswithcooperativebreeders,the in human social groups as cooperative breeding (Burkart
human strategy of reproduction and child rearing is distinct et al., 2009; Hrdy, 1999, 2009; Meehan et al., 2014). To be
from that of most cooperative breeders. We argue that the ‘‘cooperative’’ in breeding is often defined to mean that
humanspeciespracticesbioculturalreproduction.Biocultural individualsofaspeciesliveingroupsandthatmembersofthe
reproduction describes a suite of biological and sociocultural group help to feed, care for or protect offspring that they did
adaptations, including: (1) cognitive capacities for non- not bear (Burkart et al., 2009). Individuals providing these
geneticallybasedmarriageandkinshipbehaviourthatprovide services are called alloparents. Another commonly cited
demographically and ecologically flexible, but culturally criterion is that the provisioning, care and protection that
universal, alloparental care for offspring, (2) a life history alloparentsprovidemustcomeatsomecosttothealloparents.
phase of childhood, characterized by the absence of nursing That cost may be measured in assisting others to gain access
but considerable ongoing nutritional dependence, creating to food or in terms of reducing the alloparents’opportunities
extendedopportunitiesandneedsfor theprovisionofcareby to reproduce (Lukas & Clutton-Brock, 2012; Solomon &
individuals other than the parents, (3) early weaning, leading French, 1997).
CooperativebreedingspeciesarenotcommonintheOrder
Primates and, indeed, marmosets and tamarins of South
Correspondence: Barry Bogin, School of Sport, Exercise & Health
America are the only widely-recognized species of coopera-
Sciences, Loughborough University, Loughborough, UK. Tel: 44
(0)1509228819.E-mail:[email protected] tive breeding non-human primates (Fite et al., 2005;
DOI:10.3109/03014460.2014.923938 Human biocultural reproduction 369
Garber,1997;TiradoHerreraetal.,2000).Someofthecosts infants who died due to the practice of using allomaternal
incurredbymembersoftheseNewWorldmonkeyspeciesare wet-nursesin17thand18thCenturyEurope.Unlessemployed
that only a few females in a social group reproduce, two or or enslaved by wealthy families, these wet-nurses often
more males mate with the same female, which reduces male provided too little milk to too many infants, under neglectful
reproductive success and mothers without sufficient alloma- conditions, resulting in high infant mortality.
ternal support abandon or kill their dependent young
(Culot et al., 2011).
Humans are not cooperative breeders
Ethnographic work among contemporary human foragers
provides detailed examples of the extent of cooperative In surveys of the literature on breeding systems, Clutton-
allocare and its role in human societies and also shows that Brock (2002) and Hrdy (2009) reported that between 5–10%
thiscarecomesatacosttothecareprovider.Asoneinstance, of mammalian species are cooperative in breeding. Building
Marlowe(2010)reportedthatduringthefirstyear thatHadza ondecadesofresearch,Hrdy(2009)andothers(e.g.Kramer,
womenarebreast-feedingacurrentinfantthemothers’ability 2011;Meehanetal.,2013)makethecasethathumansarethe
to produce food is reduced to an average of 1713kcals/day. only species of cooperatively breeding ape. In a recent
This compares to an average food production of 3016kcals/ systematic review, Lukas and Clutton-Brock (2012) provided
day for womenwithout offspring less than 8 years old. Food a framework for characterizing breeding systems that recog-
contributions of married men increased from an average of nizes only 1.8% of mammal species as cooperative breeders
2990kcals/day to 3851kcals per/day during the first year of and, in contrast, they do not include humans among these
4 breast-feeding by their wives. The women’s decrease in food species. They make a distinction between cooperative
1
16/ productivityaverages1307kcals/dayandtheincreaseoffood breeders, communal breeders and social breeders, with
6/
0 provisioning by husbands averages only 861kcals/day. The cooperatively breeding species being those in which most of
n
6 o shortfall of 446kcals/day is made up by increased provision- the females do not breed regularly and instead provide
7
3. ing by other members of the camp, especially maternal alloparental care to the offspring of a breeding female
3
0.2 grandmothers of the nursing infant (Hawkes et al., 1989, (typically only one) to whom they are genetically related,
2
2 1997; Marlowe, 2010). These are important intergenerational oftenassiblingsorhalf-siblings(seeLukas&Clutton-Brock,
8.
y 9 resourcetransfersbetweenalloparent,motherandchildwhich 2012 for details). Humans clearly do not meet this definition
b
m carry non-trivial and measureable costs for the alloparents. asvirtuallyallwomenintraditionalforager,horticulturaland
e.conly. More detailed discussion of the importance of human inter- pastoralsocietiesreproduceregularlyiffecund(Bogin,2001).
care o generational transfers may be found in Kaplan and Robson Lukas and Clutton-Brock (2012) define other characteristics
ahealthonal us (20I0n2)aannodthGerurevxeanmeptlea,l.M(2e0e1h2a)n. et al. (2013) report that, omfoncoogoapmeroautisvebreberdeeindgingandspebciireths,ingsucohf laistternseaor-fexacllturisciivael
ormpers among Aka, tropical forest foragers living in the Central young, and interested readers may consult their article for
m infFor African Republic, mothers with children 535 months old further details. Only nine species of non-human primates
o were observed and quantitative measures of the mothers’ (1.5% of the 612 total primate species listed at http://
d fr energyexpenditurewerecalculated.Assistancetomothersby www.alltheworldsprimates.org/Home.aspx), all members of
e
d
oa alloparents significantly reduced mothers’ working energy the New World Callitricidae (marmosets and tamarins), meet
wnl expenditure by up to 216kcal during the 9-hour observation all of their criteria for cooperative breeding.
o
D period. Assistance from grandmothers provided a one-to-one Lukas and Clutton-Brock (2012: 2151) define communal
Biol exchangeofmaternaldirectcare,whiledirectinfantcarefrom breeders as those species in which, ‘‘... most adult females
m fathers decreased maternal care by almost 4 to 1. breed regularly and share care such as allonursing or feeding
u
n H In a review of 45 studies of mostly natural fertility offspring...’’. They identified four species of primates as
n
A societies, Sear and Mace (2008) found universal evidence of communal breeders (two New World monkeys and two
assistance in rearing offspring, leading them to suggest that lemurs). They do not include Homo sapiens in their list of
alloparenting is a human universal. They also found that the communal breeders because in communal breeding species
benefitsofalloparentingvariedgreatlyandoftendependedon thefemalesareclosegeneticrelatives,usuallysisters orhalf-
the kinship relation. Assistance from maternal grandmothers sisters, as the females remain in their natal social group.
and siblings living with the mother tended to improve Human alloparents may be close genetic relatives, but often
offspring survival rates. Assistance from paternal grand- are not due to the variety of post-marital residence patterns.
mothers was associated with both greater offspring survival Surveys of traditional foragers and non-foragers find that
and mortality, depending on the population, whereas help human societies most often permit bilocal residence (either
from fathers showed benefits in only about one-third of the withthewife’sor thehusband’ssocialgroup)andmostoften
studies. Sear and Mace mention the likely importance of practice patrilocal post-marital residence (with the husband’s
matrilocal vs patrilocal residence as a determinant of these social group)—matrilocal residence is least common
costs and benefits, but do not provide a formal analysis. (Alvarez, 2004; Marlowe, 2010).
Theseexamplesillustratethat,whileallocareisubiquitous Lukas and Clutton-Brock (2012) define social breeders as
in human societies, the benefits vary widely across societies. species in which the females live in groups and virtually all
In some instances, what may seem to be alloparental care breed, but rarely, if ever provide allomaternal care to others.
may, in fact, involve costs to the recipient that could detract The majority of the non-human primate species are social
from reproductive success (Digby et al., 2007; Hrdy, 2009). breeders. It is important to emphasize that the ranks of the
Hrdy (1999, 2009) described the loss of tens of thousands of socialbreedingspeciesincludealloftheAfricanapes,which
370 B. Bogin et al. AnnHumBiol,2014;41(4):368–380
are closest phylogenetically to humans. Humans, in contrast, stage evolved is not knownwith precision, but some level of
are not social breeders, as alloparental care is the rule in extensionofthepre-adultperiodofdevelopmentmayalready
human societies. have occurred about 2 millionyears agowith the appearance
of the genus Homo (Bogin & Smith, 2012). It seems likely
Human biocultural reproduction vs cooperative and that some form of genetically-driven cooperative/communal
communal breeding breeding strategy would have been necessary to sustain the
evolution of childhood and its increased requirements for
Humans certainly show cooperative and communal assist-
prolongedandmoreintensivecare,althoughthesedetailsmay
ance,supportandmutualaidinrelationtoreproduction,care
notbereconstructedbaseduponcurrentfossilevidence.What
of pregnant women and the rearing of offspring. Indeed,
does seem clear is that, over evolutionary time, the bonds of
humans have been called ‘‘super cooperators’’ in these
geneticrelatednesswhichlikelyinitiallyfosteredtheancestral
regards(Nowak&Highfield,2011).LukasandClutton-Brock
hominin strategy of raising offspring was replaced with the
(2012) observed that, as none of the African apes practices
currentflexible,culturallybasedsystemsofkinshipandmar-
either cooperative or communal breeding, it seems probable
riage that prescribe that a range of individuals provide care.
that these cooperative tendencies in raising offspringevolved
Burkartetal.(2009)proposedthatcooperativebreedingby
in hominins after they split from the last common ancestor
humanancestorsfacilitated theevolutionof largerbrainsand
with living apes. They are not original in this proposal, as it
cognitive development. Lukas and Clutton-Brock (2012)
was also offered by Hrdy (1999, 2009) and Burkart et al.
seem to reject this proposal as they find no evidence of an
(2009). We agree that the ‘‘super cooperation’’ practiced by
4 association between cooperative breeding and brain size in
1
16/ humansisanevolutionarilyderivedtrait.Wediffer,however, mammals, especially primates, and cite Iwaniuk and Arnold
6/ from Hrdy and Burkart et al. in that they equate the human
0 (2004) for the lack of such an association in corvid birds.
n styleofreproductionwithcooperativebreedinginnon-human
76 o mammals, whereas we find fundamental differences that set Alternative proposals are that other selection pressures,
3. perhaps related to greater reliance on stone tools, the use of
3 humanreproductionapartfromanyothertypeofcooperative/
20.2 communal breeding. fire and other extractive technologies (Wells & Stock 2007),
2 thedevelopmentof languageskills(Locke&Bogin,2006)or
8. We feel that the most important difference between the
by 9 humansystemandthatofnon-humancooperativebreedersis the increasing size and complexity of social groups (Dunbar,
m 2003) initiated brain/cognitive expansion. All of these
ahealthcare.coonal use only. ttruhraparaonetnsitfnheergosetphnirseeortovicsfistpeieonkcniinuiennsg.ctoHoouufpsmhlueuapdmnpsfoa,rrnootmfaclalgonoeudcnraserehtei,ecarlpenrledylarrtatoeeilsdaaentgeedrdsesear.petTeseonhxuditsreecnniestt ptihrnraeovntpeodooswlafopiltssrhtoeiadnrreuetdchtesiopahnelo,cloumfploaiarntraiiegvnneintl,iignnbgeauantgdaeanlstdloocwaissaaoslrudcrmieaglleraetiaacotnoenorsepcvweoorhoaluiptciteohironanmtaioarinyyn
ormpers offspring, but human alloparenting is unusual, perhaps even reproduction.
m infFor uanndiqupero,vaimsioonnginmg.amThmearlsesitnrircetiloyningofonbrmeeadniyngnoton-uksinuaflolyrcoanree The transition to biocultural reproduction may have co-
o evolved with the biological, behavioural and cognitive
d fr female and one, or only a few, males amongst cooperative characteristics which coalesced with the appearance of
de breeders (Lukas & Clutton-Brock, 2012) leaves the siblings
oa Homo sapiens. We have argued elsewhere that the evolution
wnl and half-siblings of the breeders with little choice for direct oftheadolescentlifehistorystageandfullsymboliclanguage
o fitnessenhancement.Hamilton(1964)formallyidentifiedthe
D are coincident with Homo sapiens (Bogin, 1999; Bogin &
Biol next best strategy, which he called inclusive fitness. By Smith, 2012). Dental evidence indicates that key features of
m assisting their close genetic relatives, the non-breeding the growth pattern of childhood were likely in place by
nn Hu aglelnoopmareenstusrvhievlepitnotehnesirurcelotsheatgecnoeptiiecskoinf.parts of their own (cid:2)160000 years ago in Homo sapiens (Smith et al., 2007).
A Adolescence, full symbolic language, systems of marriage
In the following section we show that human care and
and non-genetic kinship determination probably have more
provisioningfortheoffspringofothersisnotgovernedbythe
recent evolutionary origins, although exact dates are impos-
close genetic relatedness found in all cooperative breeders,
sible to specify with current evidence.
but is structured by sets of local, culturally-defined rules,
hence our new term, biocultural reproduction. We begin our
discussion with a brief review of the life history character- Childhood and biocultural reproduction
istics of humans that underlie the capacity and, indeed, the
Although many of the evolutionary details remain uncertain,
need for a strategy of reproduction based upon flexible,
the eventual evolution of the childhood stage in hominin
culturally-defined rules, rather than a strict adherence to
evolutionlikelyco-evolvedwithhumanbioculturalreproduc-
genetic relatedness.
tion.Humansarehighlyunusualamongmammalsinweaning
offspringbeforetheyarenutritionallyindependent.Extensive
Derived traits of human life history
provisioning of dependents by genetic kin and genetically
Theevolutionofaprotractedperiodofchildhooddependence unrelatedindividualsallowshumansto‘‘stack’’offspringand
in hominin evolution greatly expanded opportunities and spread the burden of provisioning across alloparents, thus
needs for care to be provided beyond parents and immediate facilitating both relatively high fertility, despite the intensity
kin (Bogin, 1999). The place of childhood in the stages of of investment, and high survival of each offspring
human ontogeny is given in Table 1 and Figure 1. When in (Bogin, 1999; Gurven & Walker, 2006; Hill & Hurtado,
evolutionary history and with which species the childhood 1996; Hawkes et al., 1998; Kaplan et al., 2000).
DOI:10.3109/03014460.2014.923938 Human biocultural reproduction 371
Table1. Stagesinthehumanlifecycle(modifiedfromBogin1999).Thedurationofeachstageisamedianormodalvalue.Thereissomevariation
abouttheseaveragevaluesinhealthyindividuals,especiallyfromtheInfancystageonward.Literaturesourcesfor theconstructionofthistableare
giveninBogin(1999).
Stage Duration Events
Firsttrimesterofpregnancy Fertilizationtoweek12 Embryogenesis
Secondtrimesterofpregnancy Months4to6 Rapidgrowthinlength
Thirdtrimesterofpregnancy Month7tobirth Rapidgrowthinweightandorganmaturation
Neonatalperiod Birthto28days Extra-uterineadaptation,mostrapidrateofpost-natalgrowthand
maturation
Infancy Month2toendof lactation Rapidgrowthvelocitywithsteepdecelerationinvelocitywithtime,
(usuallyby36months) feedingbylactation,deciduoustootheruption,manydevelop-
mentalmilestonesinphysiology,behaviourandcognition
Childhood 30–36monthsto6.9years Moderategrowthrate,weanedbutdependencyforfeeding,mid-
growthspurt,eruptionoffirstpermanentmolarandincisor,
cessationofbraingrowthbyendofstage
Juvenile 7–10(girls)or12(boys)years Slowergrowthrate,capableofself-feeding,cognitivetransition
leadingtolearningofeconomicandsocialskills
Puberty Brain:9–10years Inthebrain,pubertyisaneventofshortduration(daysorafew
Body:girls10years,boys12years weeks)thatreactivatesthehypothalamicGnRHpulsegenerator
leadingtoamassiveincreaseinsexhormonesecretion;onthe
body,pubertyisnotedbyadarkeningandincreaseddensitypubic
14 hair
6/ Adolescence The5–8yearsfollowingonsetof Adolescentgrowthspurtinheightandweight,permanenttooth
1
6/ puberty eruptionvirtuallycomplete,developmentofsecondarysexual
0
n characteristics;socio-sexualmaturation,intensificationofinterest
o
6 andpracticeinadultsocial,economicandsexualactivities
7
3. Adulthood
3
2 Primeandtransition 18–20yearsforwomento45years Commenceswithcompletionofskeletalgrowth;homeostasisin
0.
2 (endofchild-bearing)andfrom physiology,behaviourandcognition;menopauseforwomenby
2
8. 21–25yearsformento(cid:2)50 age50
9
y years
b
m Women’spost-reproductive 10–20yearsfollowingmenopause Bioculturallydefinedstageofwomen’slife,oftencharacterizedby
care.coe only. Oldageandsenescence Fromendofchild-bearingyearsto Decignlrivanenesdtcimnheitlnhdtersefnoufntcitmioenaanndderneepragiyrainbiltihteycoafrimnganfyorboddauygthistesursesanodr
healthnal us Death death systems
ao
ormpers
m infFor
o Human reproductive behaviour increases genetic fitness of
d fr parentsover thatofanyotherapebyenablingwomentogive
e
d
oa birth to new offspring while allowing existing dependent
wnl offspringtoreceivecareandfeedingfromclosekinandother
o
D members of the social group (Bogin, 2001, 2006). The
Biol evolution of human childhood may be viewed as critical to
m this human reproductive strategy.
u
H
n The biological constraints of childhood—including an
n
A immature dentition, small digestive system and a calorie-
demanding brain that is both relatively large and growing
rapidly—necessitate care and feeding from older individuals,
which greatly expands the opportunities for allocare within
human societies. Although women tend to provide the
majority of care to infants for at least 3 years in most
Figure 1. Distance and velocity curves of growth for healthy, well- traditional societies (Sear & Mace, 2008; Marlowe, 2010),
nourishedhumans.Boys,solidline;girls,dashedline.Thesearemodal many other individuals are also involved in the care, provi-
curves based on height data for Western Europe and North American sioningandsociallivesofinfantsandyoungchildren.Indeed,
populations.Thestagesofpost-natalgrowthareabbreviatedasfollows:
by the stage and age at which human mothers tend to wean
I, infancy; C, childhood; J, juvenile; A, adolescence; M, mature adult
(modifiedfromBogin1999).Thedistancecurve(righty-axis)indicates their infants, which is, on average, between 30–36 months in
theamountofheightachievedatagivenage.Thevelocitycurve(lefty- forager and other subsistence societies (Bogin, 2001;
axis)indicatestherateofgrowthatagivenage.Growthvelocityduring Marlowe, 2010; Walker et al., 2006), a greater percentage of
infancyisrapidwithasteepdeceleration.Childhoodgrowthisrelatively
the care of offspring tends to be provided by other family
constantat(cid:2)6cmperyear.Growthrateslowsduringthejuvenilestage
and then accelerates during the first phase of adolescence—the members including fathers, older siblings, aunts and grand-
adolescent growth spurt.Growth rates decline duringthe secondphase mothers(Gettleretal.,2011;Hawkesetal.,1998;Hrdy,1999;
untilallgrowthinheightstopsattheonsetoftheadultstage.Theimage
Kramer,2005;Meehanetal.,2014;Valeggia&Ellison,2004).
ofthe‘‘family’’isnotmeanttopromoteanyparticulartypeoffamilyas
The point we make again here in order to re-enforce its
desirable or normal, rather the cartoon figures illustrate the stages of
humanlifehistorybetweenbirthandadulthood. importance is that,althoughgenetickinare clearlyimportant
372 B. Bogin et al. AnnHumBiol,2014;41(4):368–380
as care providers, in most human societies family members characteristics, such as the cognitive capacities that allow for
with no close genetic relationship and non-family members what is often described as ‘‘theory of mind’’ (Premack &
also play crucial roles in the cooperative care and feeding of Woodruff, 1978). This phrase is often taken to mean the
children. For instance, recent work among Hadza foragers abilityofoneindividualtoimputeorattributementalstatesto
found that physical proximity and genetic relatedness self and to others. To have ‘‘theory of mind’’ requires an
explained about equally the likelihood of cooperation, appreciationthatothersmayhavedesires,intentionsorbeliefs
including childcare, between individuals (Apicella et al., that may be different from one’s own and, based upon this
2012). Indeed, all human social groups include a variety of appreciation, the ability to predict behaviour on the basis of
childcare and feeding arrangements which make use of both suchstates.Therearedebatesastowhichanimalspecieshave
biological kin and socially-defined relationships such as ‘‘theory of mind’’. We do not enter into these debates here;
in-laws by marriage, fictive kin, servants, friends or employ- ratherweacceptthatlivinghumanshavea‘‘theoryofmind’’
ees paid in cash or kind (Lancy, 2008). andrelatedbehaviourswhichsurpassthoseofotherprimates.
With these sources of childcare assistance, humanwomen We also assume that these human cognitive and behavioural
may reproduce every 2–3 years without sacrificing their own capacities evolved or were at a minimum augmented
health or the health of their current offspring. In contrast, substantially, since the hominin split from the last common
chimpanzees have a median interval of 5.9 years between ancestor with chimpanzees, without speculating on when or
successful births, that is, between births where the infant how this occurred.
survives for at least 4 years (Emery Thompson et al., 2007). Human ‘‘theoryofmind’’emergesduringdevelopmentin
4 In some traditional, non-contracepting human groups there a sequence from infant to child, juvenile, adolescent and
1
16/ may be a birth every 3 years over a 20-year reproductive adult.Twoofthecrucialchangesincognitionwhichunderlie
6/
0 career (Bogin, 2001; Lee & Kramer, 2002, see discussion theory of mind emerge at the transition from human infancy
n
6 o below). The resulting assemblage of six or seven dependent to childhood, at (cid:2)3–4 years of age. These are the capacities
7
3. offspring range in maturational status from infant to child, for pretense andthe attributionoffalsebelief inother people
3
0.2 juvenile, adolescent and even young adult (see Table 1 for (Baron-Cohen, 1995; Leslie, 1987). Bananas provide an
2
2 chronological ages). These ‘‘litter-like’’ assemblages of example of pretense. Infants accept only the reality of the
8.
y 9 offspring are both a cause and consequence of the socially banana as a fruit that may be eaten. Children are capable of
b
m diverse sources of alloparenting afforded by biocultural the pretense of a banana as a telephone or some other
e.conly. reproduction. imagined object. A common test for false belief is to allowa
care o child and another person to see a banana hidden in a basket.
ahealthonal us The nature of human biocultural reproduction Thihdedeonthinerapbeorxsoanndththeennltehaeveosthethreperrosoomn;retthuernbsatnoatnhaeriosorme-.
ormpers Aspracticedbyhumansocieties,bioculturalreproductionmay Infantsandyoungerchildrenwillexpectthattheother person
m infFor be defined as the set of marriage and kinship based rules for knowsthatthebananawasre-hidden.Childrenwiththeoryof
o extra-maternalcooperationintheproduction,feedingandcare mindwillmaketheattributionoffalsebeliefandsaythatthe
d fr ofoffspring.Thehumanstrategyofreproductionandoffspring other person thinks that the banana remains in the basket (a
e
d
oa care, which is based on both genetic and non-genetic graphic explanation isavailableat http://labspace.open.ac.uk/
wnl relationships, is distinct from that of all other mammals, mod/resource/view.php?id¼482989).
o
D including our closest genetic cousins the African apes. It is With these new abilities, the child may use pretense and
Biol vitally important to state here that we are not discussing attribution of false belief in many contexts. A kindly
m humanmating,whichtakesplacewithinandoutsideofstable neighbour may be called an ‘‘aunt’’, while two unrelated
u
H
n pair bonds and marriage. Instead, we focus on the cultural but socially-close girls may call each other ‘‘sisters’’. Older
n
A rules for the care and provisioning ofoffspring, regardless of individuals also make use of pretense toward the child, as
thegeneticrelationshiptothecaregivers.Our pointisthat,in illustrated by the kindly neighbour accepting the kinship
every human society so far observed, or for which historical name of ‘‘aunt’’ as well as the associated responsibilities for
recordsexist,therearebioculturalrulesfortheextra-maternal allocare,eventhoughsheisgeneticallyunrelatedtothechild.
(alloparental) care of dependent offspring. This is especially Many of the human social rules for alloparental care of
the case for traditional societies, which include foraging offspring are a ‘‘pretense’’ of the genetic relatedness which
groups, pastoralists and horticultural societies, but it is also drives cooperative breeding in other species. In the larger
true for nation-states based on intensive agricultural or social arena of human behaviour, these types of pretense and
industryandcontemporary post-industrialstates. falsebeliefsareessentialsupportsfortherulesforkinshipand
Marriage and kinship based rules include delegating marriage. The essential point is that, in the human species,
responsibilities for feeding, clothing, housing and educating relationshipsdefinedbymarriageandkinshiprulesoftentake
theinfants,childrenandyouthofthesocietyandoftensimilar the place of genetic closeness.
rules for the care of women of reproductive age. The rules Humans, of course, build on the foundations of primate
mayextendtoresponsibilitiesofalloparentsforarrangingthe biology and psychology that foster intimacy between mother
marriage ofoffspring. and offspring (Hrdy, 2009; Konner, 2010; Okamoto-Barth,
Abovewespeculatedthathumanchildhoodandbiocultural unpublished). These foundations are necessary for human
reproduction co-evolved as derived characteristics of our biocultural reproduction, but the degree of mother–offspring
species. In addition, human biocultural reproduction intimacy in non-human primates would not likely be suffi-
likely also required the evolution of other human-specific cient to sustain the more complex and expansive human
DOI:10.3109/03014460.2014.923938 Human biocultural reproduction 373
networks of affection and alloparental care that extend to cultures prescribe monogamous marriages, (cid:2)80% permit
manykinandnon-kin.Adeeperabilitytoimputeorattribute polygynous marriage and the remaining 2% permit polyan-
mentalstatestoselfandtoothersisrequired.Tomaselloetal. drous marriage. In practice, the most common form of
(2005) proposed that this new, deeper ‘‘theory of mind’’ is marriageisonemanwithonewoman,onaccountoftheoften
found only in the human species and theylabel it as ‘‘shared highmaterialresourcecostsofmarriagetomultiplepartners.
intentionality’’. To evolve from communal or cooperative Marital dissolution due to death, divorce (legal or de facto)
breeding to the human practice of biocultural reproduction and abandonment is known in all human cultures and re-
would have required the new emotional capacities of shared marriage is also common. This leads to ‘‘serial monogamy’’
intentionality. and polygynandrous mating, with both men and women
Goldschmidt (2006: 47) went further and emphasized the having multiple marriages or mating partners.
importance of another human emotion called ‘‘affect Human marriage is one basis for kinship determination,
hunger’’,whichhedefinedas‘‘...theurgetogetexpressions although there are others. Human societies define kinship
of affection from others’’. For humans this often means relations on the basis of familial and social ties. Humans are
affection from many others. Konner (2010) discussed theonlyspeciestouselanguageandtheculturalinstitutionof
examples of the importance of affection with many people, marriagetodefinekinshipcategories.Theapplicationofnon-
in addition to the mother, for the healthy development of biologicalcriteriaresultsinwhatissometimescalled‘‘fictive
human children in forager societies. Especially noteworthyis kinship’’,theapplicationofkinshipnamestopeopleunrelated
the affection between children with members of the social bymarriageorgeneticdescent.Fictivekinshipcanattimesbe
4 group who serve as alloparents and also as teachers of a tie between people which is as strong, or stronger, than
1
16/ essential survival skills. These people may be quite distantly biological kinship. Because the social nature of human
6/
0 related to the child in any genetic sense. kinship often overrides biological descent, some anthropolo-
n
6 o Hrdy(2009,inpress)focusesonthewaysinwhichintense gists avoidmakinganydistinction(Carsten,2000;Schneider,
7
3. alloparenting by human ancestors ‘‘changed our minds’’, 1984). Here, we use the distinction to emphasize the
3
0.2 reflecting the fact that infant attachment was spread across integrated biocultural nature of human reproduction and
2
2 many alloparents rather than just the mother. She provides alloparental care.
8.
y 9 evidence that having a broader range of alloparents and Within the context of human biocultural reproduction,
b
m attachments changes mental phenotypes and promotes the fictive kinship serves to enhance social relations including
e.conly. ability and desire to adopt the mental perspective of others affection,concern,obligationandresponsibilitytowardseach
care o (i.e. ‘‘theory of mind’’). Hrdy (2009, in press) also proposes other’soffspring.Our previousexamplewascallingtheclose
ahealthonal us tphraotmothteedntehwoseemhoutmioannalcocgapnaitciviteiesacocfomhpolmisihnminenatsncweshtoicrhs fMriresndSmofitohn.e‘’‘sAmunotthMerabryia’t’hemnaaymepr‘o‘AviudnetfMooadri,a’s’upinesrtveiasdioonf,
ormpers distinguish our species from other apes. protection,giftsandother typesofparentalinvestmenttoher
m infFor Based upon these analyses, one may conclude that human ‘‘niece’’andthe‘‘niece’’isexpectedtobehaveinaccordance
o emotion and cognition are among the features that set our with the rules of interaction between family members. An
d fr species apart from other mammals, even the apes, and ethnographic example of fictive kinship in traditional
e
d
oa undergird our capacity for emotional attachments to a range societies comes from the Hadza. Each Hadza person treats
wnl of individuals other than direct genetic kin. Our ability to all other Hadza as kin (Kaare & Woodburn, 1999). Each
o
D formstrongsocialbonds,notonlywithmothersbutalsowith person knows and uses a kinship name that would apply to
Biol many other people through social institutions such as every other Hadza, irrespective of genetic relationships.
m marriage and kinship, are critical to understanding how Given the relatively small population of (cid:2)1000 Hadza
u
H
n biocultural reproduction operates. (Marlowe, 2010), this kinship naming may not seem unusual
n
A as it is possible for any Hadza person to know a sizeable
fraction of other Hadza. However, the Hadza practice is
Marriage,kinshipandcultureinhumanreproduction
typical of much larger societies, including much of the
Marriage is a uniquely human practice with strong ties to population of China, totalling more than 1.3 billion people.
humansystemsofsocial,economicandpoliticalorganization, In traditional Han Chinese culture it is regarded as an
aswellasmoralcodes,religiousbehaviourandotherformsof offensetorefer to,oraddress,amoresenior personorfamily
ideology (Fox, 1984; Keesing, 1975). As noted previously, relation byhis or her given name. The use of the appropriate
human mating is not confined to marriage and in some kinship term is the only acceptable form of address (Baker,
societies there is littlecorrelation between the two. However, 1979). Our point is that fictive kinship, as defined anthro-
allhumansocietiespracticemarriageand,alongwithsystems pologically, is a common way that people in all human
ofkinship,theseculturalbehavioursarethecentralorganizing societies structure relationships, especially those for the
principlesforalloparentalcareinsmallscalehumansocieties, transfer of allocare, education, material resources, wealth
which collectively describe human social organization for and status.
more than 99% of the evolutionary history of Homo sapiens. Some cross-cultural examples where fictive kinship is
Itwaswithintraditionalsmall-scalesocietiesthatthebiology an essential feature of social organization include:
of childhood and the cultural power of marriage and kinship (1) Compadrazgo in Latin America (Foster, 1953), where
fostered the emergence of human biocultural reproduction. friends become ‘‘co-parents’’ of each other’s offspring,
Based on a survey of 563 mostly traditional human (2) adoption and foster care in most human cultures, by
societies, Murdock (1981) found that (cid:2)18% of human which biologically unrelated infants and children are treated
374 B. Bogin et al. AnnHumBiol,2014;41(4):368–380
as biological kin by the adopters, (3) cultures practicing Costs and fitness in biocultural reproduction
Hawaiiankinshipterminologywhere,forexample,allwomen
These examples, and hundreds of others described in the
ofone’’smother’’sgenerationarereferredtowiththekinship
literatureoncross-culturalkinshipresearch,showthathuman
name of ‘‘mother’’ and (4) the military of many nations
biocultural reproduction is based upon social relationships
where soldiers call each other ‘‘brother’’ and, in some cases,
that are qualitatively distinct, in their definition, extent and
wherenewrecruitsare ‘‘twinned’’with anoldersoldier.It is
complexity,fromthoseofcooperativeorcommunalbreeding
also common for anthropologists conducting fieldwork to be
systems.Humankinshipandmarriagesystemscastnewlight
given a kinship name by their hosts. Doing so defines,
on Hamilton’s Rule for the evolution of cooperation and
justifies and facilitates social relationships. Well-known
cooperative breeding (Hamilton, 1964). Hamilton’s Rule is
ethnographic examples are provided by Lee (1979), who
expressed as C5rB; where C is the cost in fitness to the
livedwiththe!Kung(orJu/’hoansi),foragersofNamibia,and
actor, r is the genetic relatedness between the actor and
by Chagnon (1992), who lived with Yanomamo¨, a horticul-
therecipientandBisthefitnessbenefittotherecipient.Ifthe
tural and foraging society of South America. Similar fictive
reproductive cost to the actor is less than the product of
kinshipdesignationsweregiventothepresentauthorsduring
genetic relatedness multiplied by the reproductive benefit to
fieldwork in Guatemala and the Philippines. Bogin was
the recipient, then a ‘‘helpful’’ behaviour toward the recipi-
adopted as the ‘‘son’’of a middle-class family in Guatemala
ent’s reproductive success is expected to be favoured by
City, while Kuzawa is treated as a ‘‘son’’ by someone from
natural selection. If reproductive costs are greater than the
the neighbourhood in Cebu City where he has lived in
product of rB, then apparently altruistic behaviours such as
4 the Philippines. These fictive kin designations came with
16/1 much of the affection and the responsibilities of biological alloparentingwillneverevolve.Ourreviewshowsthathuman
6/ biocultural reproduction is a system of alloparenting which
0 kinship.
n violates Hamilton’s Rule in that alloparents often incur costs
o
76 greater than the product of rB because, unlike in other
3.
3 Human social groups are based on social kinship cooperating species, the genetic relatedness between the
2
20. human actor and recipient is often small or, essentially, zero.
2 Hill et al. (2011) surveyed 32 present-day foraging societies,
8. Asthevalueof‘‘r’’approacheszerothecostsofalloparenting
by 9 includingthe!Kung(Ju/’hoansi),theAcheofSouthAmerica far exceed the benefits. In reality, the cost in fitness to the
m and the Hadza and reported that human hunter-gatherer
e.conly. societies have a social structure that is unique among all aplalrotpaorfenetlabbeocroamteeksiqnushitiepdnifeftiwcuolrtktsoamndeafsaumrei,liaesstchreeaatcetdorbiys
m informahealthcarFor personal use o piggwnreroainrmmneedstaeiiptncdeaaesrln.oelytHnfitaislldr.leigselTraptohteaeuirlsdps.isfinosbwguydenruodederteghstreaocentem,entohtatinecinafaiplrvnloryegamrcuatniginccreeeo,ltm7ahb5temye%idrobonoonfrtahiaptntaadmlrlieeveanginstdrstouanuanoopldsrt. mrriateenislaodaorntruesibradecegnneneeset,safsiii.wltnesEhdiwwqcbuhhayayiclkslshyitnrtushmihmcaaittpupyrodcerooatfattfenhsngteeo,ottrtifhaelaneoslywwroeabmsyolusiaflgttaemeitrnniiaoaepenlrmgsooyorantnitaobodnniodapglloreoocgnhtoiehcistbeaitcs-rl
o Migrations to new groups dilute genetic relationships and
d fr require social kinship designations to help structure new costs. The fitness benefit (B) to the recipient also becomes
de more complicated to measure for the same reasons. In
wnloa rkeilnasthioipnsahrirpasn.geInmeonutsr, vwihewic,h tohpeesreatetypinesadodfitisooncitaollyg-ebnaesteidc addition to the metrics used to understand evolutionary
o selection pressures in non-human animals, such as survival,
D kinship, are the essence of what sets human biocultural
Biol reproduction apart from the forms of cooperation found in ginrvoowlvthesannodn-fbuitoulroegirceaplrcoodnutcrtiibount,iohnusmtoantherepmreomdubcetrisonofatlhsoe
m other species. Hill et al.’s findings complement and extend
u social group, such as emotional affection, the teaching of
H
n those of Apicella et al. (2012), who reported that Hadza culturally acquired skills and transfers of material goods and
n
A camps are comprised of people with distant genetic relation-
other wealth (Gurven et al., 2012). In these ways, biocultural
ships:firstordergeneticrelativescomprisedlessthan10%of
reproduction differs from cooperative and communal breed-
residential camps.
ing because it not only contributes to the inclusive fitness of
Peoplewill marry and reproduce according to the rules of
parents and genetically-related helpers, but it also serves to
kinship, often with disregard to their degree of genetic
continually reproduce and recreate the social, economic,
relationship.Lee (1979)foundthat!Kungregard peoplewith
political and moral cohesion of social group members.
the same name as equal in kinship. A man will regard all
womenwiththesamenameashissisterasasister.Marrying
Why do humans rely upon such diversity in kinship
a sister is forbidden, so all women a man calls sister are
and allocare strategies?
unmarriageable.
Chagnon (1992) reported that the Yanomamo¨ practice a One hallmark of the human system of biocultural reproduc-
type of kinship classification by which a man calls his tion is extreme flexibility. Local ecological conditions vary
mother’s sisters and some other women by the kinship name across the range of environments that traditional subsistence
‘‘mother’’.Thedaughtersofthese‘‘mothers’’arenoteligible level human societies inhabit today and have inhabited for
formarriage.Ashortageofeligiblewomenisoftenaproblem millennia. It is likely that the effective patterns of allocare,
for Yanomamo¨ men. Chagnon described the social mechan- including kinship and marriage-defined rules for provision-
isms by which a man can change the kinship name of his ing, holding, protecting and educating the young varied
mother’s sister from ‘‘mother’’ to ‘‘mother-in-law’’, which remarkably over time and place. One well researched
thereby makes her daughters eligible for marriage. ethnographic example are the Hadza, among whom heavy
DOI:10.3109/03014460.2014.923938 Human biocultural reproduction 375
and difficult to dig tubers are a key food resource. Hadza childhood in the hominin lineage. In addition, the play
grandmothershavetheknowledgeandphysicalstrengthtodig group, in the protective environment of the home base or
them, allowing them to play a central role as allocaregivers camp, provides children and juveniles with the freedom to
(Hawkes et al., 1989). explore and experiment, which tends to encourage learning,
Another common pattern of child care in many traditional toolusing,socialization,physicaldevelopmentandemotional
cultures is to have juveniles assume caretaking responsibil- well-being (Bogin, 1999, 2002).
ities for younger children. This occurs among two well- These examples illustrate how humans, unlike other
studied African hunting and gathering societies, the !Kung species, have adopted a system of biocultural reproduction
(Konner, 2010) and the Mbuti (Turnbull, 1983a, b). In these and offspring care that is flexible and responsive to local
societies, mothers carry their infant and still nursing child opportunities and constraints. Having our kinship and mar-
(nursing a child to age 4 years is common in these cultures) riage systems, including fictive kinship and many styles of
with them while foraging. Weaned children must stay marriage practices, emerge locally, allows greater opportu-
‘‘home’’, that is at the base camp, as pre-adolescent children nities for plasticity in behavioural accommodation of local
have neither the strength nor stamina to follow their parents ecological realities. In contrast, other species that practice
while gathering or hunting. At !Kung camps children of cooperative or communal breeding have relatively narrowly-
various ages play together within the camp boundaries while constrained systems of collective care based on close genetic
juveniles discharge many caretaking functions for younger relationships.
children. The childrenseem to transfer their attachment from Wearemindfulthatthereisnosimplecorrelationbetween
4 parents and other adults to the juveniles, behaving toward types of marriage and kinship systems and local ecologies.
1
16/ them with appropriate deference and obedience. The age- Styles of human alloparental care likely developed due to
6/
0 graded play group functions to transmit cultural behaviour many historical factors that are often challenging to recon-
n
6 o from older to younger generations and to facilitate the structfromthefossilrecord.Weonlymeantoemphasizethat
7
3. learning of adult parental behaviour (Konner, 2010). Of humanalloparentalcarebasedonbioculturalrulesforkinship
3
0.2 course,thechildrenandjuvenilesareneverquiteleftontheir andmarriageresponsibilitiesprovidehumanpopulationswith
2
2 own,asthereisalwaysoneadultormoreincampatanytime, enormousflexibilitytoadapteffectivelytotheunusuallywide
8.
y 9 butthispersonisnotdirectlyinvolvedinchildcare.Rather,he range of ecologies that our species has colonized (Wells &
b
m orsheispreparingfood,toolsorotherwiseprimarilyengaged Stock, 2007).
e.conly. in adult activities.
ahealthcaronal use o cmeenTntrtha.elAAMftferbiructawin,earwanhiinnogfo,arrteeosdtnsd,olemhrasavdeeincateshriumnthitleearrswcoahrnilldddcgoaafreththaeerrrearbnsogpoei-f, Befiofocrutltural reproduction and lifetime reproductive
ormpers theMbutitermfor thechildren’splayground,butalsoaplace In this final section we tie together our discussion of the
m infFor of age-graded childcare and cultural transmission. Between biocultural nature of human reproduction and the childhood
o the ages of 2–3 years to 8–9 years of age, children and stage of life history by analysing their consequences for
d fr juvenilesspendalmostalloftheirdayinthebopi.Therethey lifetime reproductive effort (LRE) and the broader implica-
e
d
oa learn physical skills, cultural values and, even, sexual tions of these ideas for understanding the evolution of the
wnl behaviour. Turnbull (1983b: 43–44) notes ‘‘Little that chil- human life history. LRE may be defined as the metabolic
o
D dren do in the bopi is not of full value in later adult life’’. energydevotedtoreproduction,relativetomaintenancecosts,
Biol Theage-gradedplaygroupprovidesforboththecaretaking over the average adult life span. To explain this definition of
m and enculturation of the young, freeing the adults from these LREwefirstprovidebackgroundonreproductiveeffort(RE).
u
H
n tasks so that they may provide food, shelter and other Withinthelifehistorytheoryliterature,REisoftendefinedas
n
A necessities for the young who may be at various stages of includingexpendituresofenergyandtimein:(1)mating,that
development. A formal mathematical treatment of the repro- is, searching for, finding/attracting and keeping a mate(s);
ductive benefits of an age-graded division of labour for (2) offspringproduction, including gametogenesis,siringand
alloparenting was provided by Kramer (2014). The ethnog- gestating offspring along with (in mammals) milk transfers
raphyandtheformalanalysisbothshowthatawomanmaybe during infancy; and (3) parental investment, which includes
pregnant, have a child weaned within the past year and have all expenditures of the parents’ time and energy on any one
one or more older offspring simultaneously. Kramer’s ethno- offspring.Alloftheseexpendituresareviewedascomingata
graphic fieldwork with Maya horticulturalists of Mexico cost to parental abilities to invest in their own somas and in
foundthattheaverageMayawomanwillbeabletogivebirth other current—or future—offspring (Hamilton, 1964, 1966).
andrear7offspringduringa20-yearreproductivecareer(Lee Human reproductive effort is highest between the ages of
& Kramer, 2002). As children, juveniles and adolescents, 18–40 years in most societies. In traditional societies,
those offspring contribute time and labour toward the especiallyforagers,reproductivecareersaretypicallyinitiated
alloparenting of their younger siblings, cousins and others. after 17 years of age, with 19 years being the modal age at
Itisnotuntiltheoffspringare(cid:2)20yearsoldthattheyachieve first birth for women (Bogin, 2001; Marlowe, 2010). After
independenceintermsoftheabilitytoleavetheirnatalsocial about 35 years of age, women’s biological capacity to
group to begin their own families. conceive (fecundity) begins to decline slowly until meno-
As we proposed previously, the selective advantage of a pause, which can be defined as the cessation of monthly
greaternumberofsurvivingoffspringaffordedbyage-graded menstrual cycling and the absence of ovulation in adult
caretaking may, in part, account for the evolution of women. Menopause is usually reached by (cid:2)50 years of age,
376 B. Bogin et al. AnnHumBiol,2014;41(4):368–380
although there is some evidence that it may occur earlier reproductive effort (LRE) by taking the RE of an average
when women have been subjected to poor-quality environ- reproductive bout multiplied by the average number of bouts
ments in terms of nutrition, infection or heavy workloads acrossthereproductivelifespanofafemaleofthatspecies.It
(Murphyetal.,2013).Insocietiesinwhichthereisnoparity- isimportanttodistinguishLREfromarelatedmeasurecalled
specific limitation on the number of children and hormonal lifetime reproductive success (LRS). The LRS of a female
contraceptionisnotused,completedfertilityratesmayexceed equals the total number of surviving offspring that she
15 per women (Larke & Crews, 2006). Relatively high produces in her lifetime (Robbins et al., 2011). It is well
fertility likely characterized much of human history, as knownthathumanshavethehighestRSofallprimatesanda
opposed to modern high income settings in which birth RS higher than many mammals (Bogin 2001; Walker et al.,
control is common and fertility typically falls below two per 2008). In contrast, LRE encapsulates the direct metabolic
woman. Men’s reproductive success follows closely that of burdenofreproductionoverafemaleanimal’slifecourseand,
women in the same population, although in some traditional thus, is a way of expressing the total amount of energy a
settingsalargervarianceinmen’stotalfitnessisobserveddue typicalfemalememberofaspeciesallocatestoreproduction,
to inter-male competition for access to mates via aggression on average, over her lifecourse.
and/orculturalruleswhichchannelwomentoolder,wealthier Specifically, Charnov et al. (2007) express LRE as:
or more socially dominant men (Alexander & Noonan, 1979;
Chagnon, 1979; Crews, 2007; Marlowe, 2000). ðlittersperyearÞ(cid:3)ðlittersizeÞ(cid:3)ðaveragereproductivelifespanÞ
Extensive, high quality parental investment is a hallmark (cid:2)offspringmassatindependence(cid:3)
(cid:3)
14 ofhumanreproductiveeffortanditsetshumansapartfromall adultmassatfirstreproduction
16/ other mammals and other large-bodied apes (Lancaster &
6/
0 Lancaster, 1983). The intensive parental investment that Charnov et al.’s (2007) use of the word ‘‘litter’’ also
n
6 o characterizes human biocultural reproduction is made pos- includes other terms to denote birthing events, such as
7
3. sible by kinship and marriage rules, noted above, which clutches and broods. Calculating LRE for 54 lizard species,
3
0.2 organizepatternsofenergyandlabourtransfersbyalloparents they find a mean LRE of 1.43 (1.3–1.5, 95% confidence
2
2 to mothers and their offspring. This style ofalloparental care interval) and, for 40 mammal species, a mean LRE of 1.41
8.
y 9 allowshumansocietiestomaintainextremelyhighinvestment (1.2–1.6,95%CI).Noprimateswereincludedintheanalysis.
b
m in each offspring, while also allowing human women to These results indicate that, across this range of animal
e.conly. achieve the highest fertility and shortest inter-birth intervals species,withvaryinggrowthandproductionrates,theaverage
care o of all the apes (Bogin, 2001; Bogin & Smith, 2012; female ina typical mammal or lizard will generate a mass of
ahealthonal us HShrdoyrt,,11999796;).Kramer & Ellison, 2010; Reiches et al., 2009; (o2ff0s0p7r:inEg1(cid:2)351).4e-xtipmlaeisn htheartoLwRnEbiosdoyfwtheeigohret.ticCahlairmnopvoretatnacle.
ormpers because it ‘‘... is a key component of fitness... and it
m infFor Lifetime reproductive effort encompasses the central core of 40 years of life history
o thought—reproductive allocation, size at maturity, and adult
d fr Earlyhistorical‘‘seeds’’ofthemodernnotionofreproductive life span. This places it central tothe studyof life histories’’.
e
d
oa effort (RE) were planted by Fisher (1930), who formulated Following the approach developed by Charnov et al.
wnl the concept of ‘‘reproductive value’’, which he described as (2007), Burger et al. (2010) calculated the average LRE of
o
D the direct reproductive contribution that an individual of a human women using data from 17 small-scale, traditional
Biol givenage,onaverage,willmaketofuturegenerations.Fisher societies. By multiplying the average fertility rate, offspring
m wrotethatthisis‘‘...ofsomeinterest,sincethedirectaction sizerelativetomaternalbodymassandreproductivelifespan
u
n H of Natural Selection must be proportional to this contribu- ofwomenwithinthesepopulations,theycalculateanaverage
An tion’’ (Fisher, 1930: 27). Lack (1947) extended this concept LRE of 1.45 (±0.12, 95% CI). This value is statistically
when he analysed egg clutch size in birds and reported a indistinguishable from the predicted average LRE value
trade-offbetweenthenumbervssizeofoffspring,concluding calculated by Charnov et al. (2007) for other mammals,
that,‘‘Theparentalfeedingratetendstoincreaseifthebrood suggesting that humans may be typical mammals in this
is larger, but not proportionately, so that each nestling gets a regard.
smallershareofthefoodinalargethanasmallbrood’’(Lack, Whileanimportantinitialstep,theassumptionsemployed
1947: 331). Lack’s observations have been cited by subse- by Burger et al. do not fully account for the energetic and
quenttheoristsaspartoftheearlydevelopmentof lifehistory reproductive benefits accrued to human mothers through the
thinking (Ricklefs, 2000). Building on Fisher, Lack and processesofbioculturalreproductiondiscussedabove.Burger
others, Williams (1966) proposed an elegant way to express et al.’s analysis relies on the assumption that maternal per-
the propagative part of these basic trade-offs. He called this offspring RE is reflected in the size of an offspring at
‘‘Reproductive Effort’’ (RE) and defined it as that portion of nutritional independence from maternal metabolism.
adult body mass devoted to reproduction per unit time Nutritional independence from the mother is relatively
(Williams, 1966). There has been much discussion of how simple to estimate for a reptile—when the egg is laid or the
besttomeasureRE(e.g.Gadgil&Bossert,1970;Hirschfield viviparous offspring are birthed (Somma (2003) describes
& Tinkle 1975; Smith & Fretwell, 1974), but William’s some rare exceptions). For most mammals, nutritional
definition remains the most commonly used method. independence from the mother is achieved at weaning (end
Charnov et al. (2007) further extended the RE concept by of lactation). Cooperative breeding mammals are exceptions,
devising a method for estimating a species’ average lifetime assomefoodprovisioningmaybecommontoweanedyoung.
DOI:10.3109/03014460.2014.923938 Human biocultural reproduction 377
Charnov et al.’s (2007) definition of nutritional independ- proportion of infant needs met by breastfeeding will tend to
ence is central to their estimation of LRE in non-human progressively decline following peak lactation (Lee, 1996;
species. That definition of nutritional independence clearly Sellen, 2007). All of this theoretical discussion is consistent
does not apply to species with extensive nutritional transfers with empirical observations, from ethnographic research of
from alloparents. The human species is most notable in this humansocieties,oftheroleofbothmothersandalloparentsin
regard.Forhumans,weaningisnotequivalentwithnutritional providing a variety of foods to still breast-feeding infants,
independence from the mother as she is likely to continue to which can even include breast milk from wet-nurses (e.g.
supply food for many years. A further complication for Hrdy (1999) for historical sources and Tronick et al. (1987)
humansisthatbothpriortoweaningandformanyyearspost- for a contemporary forager society example). Taking such
weaning other people will supply food to infants, children, factors into consideration, Sellen (2006, 2007) has estimated
juveniles, adolescents and even adults (Reiches et al., 2009; that supplementary feeding could account for 1.8MJ/day of
Kramer&Ellison,2010).Accordingly,thedefinitionofLRE infant needs during the first year, which is the equivalent of
likely needs modification when applied to the bioculturally abouttwo-thirds(67%)oftheenergeticcostofpeaklactation.
reproducing human species. Using the same dataset as Burger et al. (2010), we re-
In their estimation of human LRE, Burger et al. treat estimated human LRE bymodifying the equationfor LRE to
humansasiftherewerenopre-weaningalloparentaltransfers. reflect these unique, species-defining characteristics of the
Burgeretal.(2010)alsoassumethattheageofindependence human life history (Bragg et al., 2012). We re-calculated
inhumansoccursattheageofcompleteweaning,whichthey LRE by ‘‘adjusting’’offspring size at weaning to reflect the
4 defineas3yearsafterbirth.Theythenusevaluesforaverage proportion of offspring weight gained from conception
1
16/ offspringweight(ingrams)atthatageforthevariable‘‘litter through size at weaning ‘‘paid for’’ bymaternal metabolism,
6/
0 size’’ in their empirical estimation of LRE. Elsewhere, we as well as the portion paid for by complementary feeding.
n
6 o have examined in greater detail these assumptions and We followed Burger et al. (2010) and assumed age 36
7
3. explored strategies for calculating LRE that account for months to be the age at weaning. We used the same data set
3
0.2 more of the features of our unique strategy of biocultural of 15 small-scale forager and traditional subsistence-based
2
2 reproduction(Braggetal.,2012).Herewepresentasummary societies. We re-calculated human LRE based on both
8.
y 9 of these considerations. ‘‘high’’ and ‘‘low’’ estimates of the energy savings afforded
b
m Across all placental mammals, three distinct phases of by complementary feeding, which were derived from the
e.conly. maternal investment in reproduction can be identified: (1) empirical data for infant energetic requirements and mater-
care o direct metabolic transfers during gestation, (2) a period of nal breast milk production. With these modifications, we
ahealthonal us enxeceldussiavree bmreeatsvtfieaebdrineagstwmheilnk aalnldo(f3)thienimnfaannyt’smanmutmritailosn,aal e1s.0ti2m–a1t.e23t,haatsstuhmeinLgREhigohf(h6u7m%a)ntowloomwe(n33is%o)nprtohpeorotriodners ooff
ormpers period of ‘‘mixed’’ feeding during which infant nutritional the energetic needs of weanlings older than 6 months
m infFor requirements are met by a blend of infant self-provisioning being met by complementary foods in lieu of breast milk
o and breast milk (Langer, 2008). The nature of this third, (Bragg et al., 2012).
d fr transitional feeding phase is greatly modified in humans Our estimates of human LRE are 14–29% lower than that
e
d
oa compared to all other great apes and non-cooperatively calculatedbyBurgeretal.(2010).Thisdifferencerepresentsa
wnl breeding primates (van Noordwijk et al., 2013a). In wild significantsavingofenergyexpendedonreproductioninboth
o
D Bornean orangutans, offspring are entirely dependent upon statistical terms and also in biological function. Statistically,
Biol milk and do not initiate self-foraging until mid-way through the difference between Burger et al.’s (2010) mean LRE of
m thesecondyearoflife,withfullweaningfrommilkoccurring 1.44 (SD¼0.22) and our conservative mean estimated LRE
u
n H at an average of 6.5 years (van Noordwijk et al., 2013b). of 1.23 (SD¼0.20) results in a t¼2.65 with p50.01.
n
A Humans, rather than shifting from milk to a combination of Biologically,ournewhumanLREvalues,rangingfrom1.02–
milk and self-provisioning, shift from milk to ‘‘complemen- 1.23,resultinsubstantialenergysavingsthatmaybeinvested
tary feeding’’ wherein still-dependent and nursing offspring in other functions or needs. These include defense against
are fed nutritionally-rich, specially prepared foods (Bogin, infection, maintenance ofthe mother’s body, food production
1999; Knott, 2001; Lancaster & Lancaster, 1983; Lee, 1996; and social interactions.
Sellen, 2006). Complementary feeding of human infants We have speculated that another life history change
generally begins (cid:2)6 months of age and often earlier, which derivedfromassociationsbetweentheevolutionofchildhood,
meansthat,for themajorityoftheperiodof lactation,infants biocultural reproduction and lower LRE may be greater
receive both their mother’s milk and foods supplied from longevity than any other primate species (Bogin, 2009;
outside the mother’s body. These complementary foods Kuzawa&Bragg,2012).Theenergysavingsinvestedinbody
should not be included in the calculation of LRE which, maintenance may have slowed the senescence of somatic
accordingtoCharnovetal.(2007),isreservedfortheamount capacities and capital and prolonged human lifespan by
of energy that mothers provide as direct metabolic transfers several decades more than our closest great ape kin (Bragg
to offspring. et al., 2012; Crews & Bogin, 2010; Gurven et al., 2012;
Thehighestenergeticoutputthatanaveragehumanwoman Kuzawa & Bragg 2012). In this way, the distinctive features
achieves during lactation is (cid:2)2.7MJ/day (Prentice et al., of human biocultural reproduction, which co-evolved with
1996; Sellen, 2007), which is already outstripped by infant the stage of human dependence known as childhood,
energy requirements at 6 months of age (Butte et al., 2000). may be directly linked with the evolution of our unusually
Because energy needs continue to increase with age, the long lifespan.