Reproductive Strategies and Primate Evolution

Research has indicated that one primary input to the encephalization levels observed in primates and other mammals relates to reproductive and life history strategies. It is necessary to review our general understanding of these mammalian and primate reproductive strategies prior to assessing these associations with encephalization, however. Building directly on previous work by Adolf Portmann (1939, 1965), Martin (1972, 1973, 1975a,b) noted that mammalian reproductive strategies could be organized into two alternative modes: altricial and precocial. The salient aspects of these alternative reproductive strategies are given in Table 3. In essence, these strategies correspond to the broader life history "fast-slow continuum" among mammals (Charnov, 1993; Charnov and Berrigan, 1993; Jones and MacLarnon, 2001; Promislow and Harvey, 1990; Read and Harvey, 1989), derived from the r-K continuum (MacArthur and Wilson, 1967) and density-dependent versus density-independent mortality rates. The altricial mode of reproductive strategy has been characterized as "living fast and dying young" and is linked to relatively high levels of natural mortality (Promislow and Harvey, 1990) and intrinsic rates of natural increase (Hennemann, 1983). These species tend to produce large litters of relatively undeveloped young after short gestation periods. Altricial species are typically small in body size and relative brain size. The tailless tenrec, Tenrec ecaudatus, from Madagascar provides one example of a highly altricial mammal (Figure 6A). This tenrec may produce litters of over 30 offspring. Precocial species, by contrast, develop more slowly and take longer to mature. They are characterized by lower levels of mortality and the production of small litters of well-developed offspring following extended gestations. Intrinsic rates of natural increase are lower in such groups (Hennemann, 1983). Precocial mammals tend to be of moderate-to-large body size, and relatively highly encephalized. The elephants provide a good example of a precocial mammal (Figure 6B).

Table 3. Alternative states for development of offspring at birth in mammals

Altricial type

Precocial type

1. Adults usually construct nests, at least when dependent offspring are present. Adult body size typically small

2. Infants are born naked, and the ears and eyes are closed by a membrane for some time after birth. Initially, the young usually exhibits imperfect homeothermy compared to adults

3. The lower jaw is incompletely developed at birth and the middle ear is hence at an early stage of development. The teeth erupt quite late in postnatal development

4. The gestation period is relatively short; litter size and teat count are large

5. Infants typically have low mobility at birth

6. The relative brain size of the neonate and of the adult is small, and the brain usually grows considerably after birth

7. The adults are generally nocturnal in habits

1. Adults do not normally construct nests at any stage. Adult body size tends to be medium or large

2. Infants are born with at least a moderate covering of hair, and the ears and eyes born with atleast a moderate are open at birth or soon afterwards. Homeothermy typically well developed at birth compared to the adult condition

3. The lower jaw is well developed at birth and the middle ear is fairly well developed. The teeth quite soon after birth, at least in small-bodied forms

4. The gestation period is relatively long; litter size and teat count are very small

5. Infants typically have high mobility at birth

6. The relative brain size of the neonate and of the adult is large, and the brain grows only moderately after birth

7. The adult tends to be diurnal in habits, though a fair number of smaller species are nocturnal

From Martin, 1975b, following Portmann, 1939, 1965; italics added; Note particularly the entries on relative brain size (# 6) and overall body size (#1).

Mammalian orders are often characterized as being either precocial or altri-cial, although "mixed" orders such as the carnivores and rodents are acknowledged (Martin, 1975a,b). However, it is perhaps not surprising that with multiple inputs into these reproductive and life history strategies, it is sometimes difficult to view mammalian species as simply one mode or the other. Derrickson (1992) assessed four criteria (thermoregulatory, sensory, locomotory, and nutritional) of offspring development and noted various intermediate or mixed groupings (see Table 4). Studies by Case (1978) and Eisenberg (1981) utilized somewhat different developmental criteria, and again uncovered taxa not easily classified as one mode or the other. Martin and MacLarnon (1985) characterized various species as "intermediate" between the precocial and altricial modes in their study of gestation length scaling. It

Precocial Mammal

Figure 6. These two taxa offer a striking contrast in mammalian reproductive strategies. A. The highly altricial tailless tenrec (Tenrec ecaudatus) has very large litter sizes, in rare cases as many as 30 or more neonates (Louwman, 1973) (with the kind permission of Blackwell Publishers); B. The strongly precocial elephant, typically bearing a single well-developed offspring (with the kind permission of David Pride).

Figure 6. These two taxa offer a striking contrast in mammalian reproductive strategies. A. The highly altricial tailless tenrec (Tenrec ecaudatus) has very large litter sizes, in rare cases as many as 30 or more neonates (Louwman, 1973) (with the kind permission of Blackwell Publishers); B. The strongly precocial elephant, typically bearing a single well-developed offspring (with the kind permission of David Pride).

Table 4. Neonatal development in 16 orders of mammals

Number of genera (families) within developmental category

Table 4. Neonatal development in 16 orders of mammals

Number of genera (families) within developmental category

Order

0

1

2

3

Total

Insectivora

9(2)

1(1)

-

-

10(3)

Macroscelidae

-

-

-

1(1)

1(1)

Chiroptera

7(2)

1(1)

3(2)

-

10(3)

Scandentia

-

1(1)

-

-

1(1)

Primates

-

2(2)

18(9)

-

20(9)

Edentata

1(1)

-

2(1)

1(1)

4(3)

Pholidota

1(1)

-

-

-

1(1)

Lagomorpha

2(1)

2(2)

-

1(1)

4(2)

Rodentia

58(9)

5(3)

4(4)

17(12)

83(19)

Cetacea

-

-

-

2(1)'

2(1)'

Carnivora

12(5)

14(5)

2(2)

1(1)

27(7)

Pinnipedia

-

-

-

4(3)

4(3)

Tubulidentata

-

-

1(1)

-

1(1)

Proboscidea

-

-

-

1(1)

1(1)

Hyracoidea

-

-

-

1(1)

1(1)

Artiodactyla

-

-

1(1)

12(5)

13(6)

Total

90(21)

26(15)

31(20)

41(27)

183(62)

From Derrickson, 1992; Developmental categories represent a scale from 0 (highly altricial) to 3 (highly precocial), quantified as a composite value based on neonatal independence in four key areas: thermoregulatory, sensory,, locomotory, and nutritional. Note that total numbers of genera and families may differ from the sum of the developmental categories, due to the fact that some taxa may be represented in more than one category.

From Derrickson, 1992; Developmental categories represent a scale from 0 (highly altricial) to 3 (highly precocial), quantified as a composite value based on neonatal independence in four key areas: thermoregulatory, sensory,, locomotory, and nutritional. Note that total numbers of genera and families may differ from the sum of the developmental categories, due to the fact that some taxa may be represented in more than one category.

is clear that continuous variation exists for mammal species in some of the factors contributing to the dichotomous precocial and altricial reproductive strategies (Zeveloff and Boyce, 1986), and much additional work remains to be undertaken in order to clarify such variation and its bases.

Primates as an order are classified as strongly precocial (Derrickson, 1992; Eisenberg, 1981; Martin, 1975a,b). The great majority of species give birth to a single, well-developed offspring with relatively large neonatal brain size, following a prolonged gestation period (Martin and MacLarnon, 1985, 1988; Pagel and Harvey, 1988). Significant variation among primate (predominantly strepsirhine) species does exist in the number of offspring, teat number, mother-infant relations, nest-using behavior, and related attributes (Martin, 1975a,b). Kappeler's (1995, 1996, 1998) studies have contributed considerably to the documentation and phylogenetic analysis of this variation. He notes that primates range from those producing the most precocial young (such as Eulemur, Lemur catta, indris, lorises, tarsiers, and the anthropoids), where neonates are very well developed and capable of grasping the mother's fur or other supports, to certain species characterized by less precocial young (e.g., Varecia and many cheirogaleids), where infants may have eyes closed at birth, exhibit difficulty with coordinated movement, and are born in litters. Some Microcebus species produce up to two litters of 2-3 rapidly growing offspring in their first year of life, and Varecia variegata, the variegated lemur, builds nests for litters of 2-3 infants. Many galago and cheirogaleid offspring are also left in nests and tree holes for some time after birth. Various primates, such as lorises, tarsiers, lepilemurs, and the wooly lemur (Avahi laniger), carry their young from birth onward, in certain cases "parking" them for brief periods while the mother forages. On a higher taxonomic level, it is a fair generalization to note that lorisids are quite precocial and slow-growing, cheirogaleids are generally less precocial with more rapid development, galagids are somewhat mixed and intermediate, with the lemurids being predominantly quite precocial (Kappeler, 1996). The data compilations and phylogenetic reconstructions for features including nest building, tree-hole use, infant oral transport, infant carrying, teat number, litter size, activity pattern, and social organization should be consulted for further information (Kappeler, 1998).

This diversity raises issues of both reconstructed ancestral states for primates, and the ecological factors underlying this observed variation. Martin (1975a,b) argued that the strong precociality of extant primates is primitive for the order, and linked to evolution in stable environments with relatively predictable resources and competition, along with low levels of neonatal, juvenile, and adult mortality. He further suggested that those primates characterized by somewhat higher rates of reproductive turnover (such as some of the cheirogaleids and Varecia variegata) had secondarily evolved these patterns in response to more unpredictable seasonal environments. Kappeler's (1998) phylogenetic reconstructions have argued that the earliest primates were nocturnal and solitary, with three pairs of teats, and a single offspring which was initially kept in a shelter (tree hole or nest) and subsequently mouth-carried to a parking place where they grasp for periods of time while the mother forages for food. This reconstructed state is similar to that seen in many extant galagids. Kappeler (1995) further stresses that although certain nocturnal strepsirhines do indeed exhibit several ancestral mammalian reproductive traits, such as multiple offspring, nest building, and infant parking, their overall life history strategies are essentially primate-like and reflect a clear evolutionary shift toward the production of quite precocial young. In sum, early primates were probably

Table 5. Life history and encephalization data for selected small, precocial mammals

Species Order; Family

Body weight (g)

Brain weight (g)

Litter size

Gestation length ( days )

IP and/or EQ'

Ekphantulus fuscipes

57"

1.33"

1-2s

60s

287"; 0.75'

Macroscelidea; Macroscelididae

Ekphantulus intufi

49 <i

l-2d

51"1

—; 0.70''

Macroscelidea; Macroscelididae

Ekpha n tu lus myu rus

64"'

l.37d

l-2d

46"'

—; 0.70'

Macroscelidea; Macroscelididae

Cyn opterus horse field ii

53f

1.24/

1-2s

115-125-"

236/; 0.72'

Chiroptera; Pteropodidae

Microcebus m urin us

54"

1.78"

l-3b

59-62-"

334";0.86'

Primates; Cheirogaleidae

Tupa ia ja va n ica

105"

2.55"

2s

315"; 0.94'

Scandentia; Tupaiidae

Tupaia jjlis

150"

3.15"

2-3-"

46-50-"

310"; 0.92'

Scandentia; Tupaiidae

Urojjale everetti

275"

4.28"

1-2*

54-56s

287"; 0.83'

Scandentia; Tupaiidae

Cheirojjakus medius

177"

3.14"

2-3s

70s

279"; 0.82'

Primates; Cheirogaleidae

Pteropus edwardsi (Wirz)

287/

8.00/

527/; 1.50'

Chiroptera; Pteropodidae

Pteropus edwardsi (Warncke)

375^

6.85/

382/; 1.08'

Chiroptera; Pteropodidae

Loris tardijjradus

322"

6.60"

lb

180s

402"; 1.15'

Primates; Lorisidae

Cheirojjakus major

450"

6.80"

2-3s

70s

336"; 0.95'

Primates; Cheirogaleidae

Chinchilla lanijjer

432"'

5.25"'

2d

110"'

—; 0.75'

Rodentia; Chinchillidae

BJiyn chocytm stuhlma n n t

432''

5.25*

2*

110*

—; 0.75'

Macroscelidea; Macroscelididae

Myoprocta pratti

780*

9.90*

1.2*

98*

—; 0.95'

Rodentia; Dasyproctidae

Otokm u r crnsskn ud at us

850"

10.30"

1 *

135*

341"; 0.94'

Primates; Galagidae

120-150"

Avahi Inniger occidentalis

860"

9.67"

1"

317"; 0.87'

Primates; Indriidae

Lepikmur ruficaudatus

915"

7.60"

ii

12a"

240"; 0.66'

Primates; Lepilemuridae

Avnhi Inniger Inniger

1270"

11.45"

1"

120-150"

294"; 0.79'

Primates; Indriidae

Hapalem u r sim us

1300"

9.53"

1 s

16a»

—; 0.65'

Primates; Lemuridae

Pteropus vumpyrus

1220"

10.20^

1"

180"

271/; 0.73'

Chiroptera; Pteropodidae

Potos flnvus

1970"'

31.20*

1.1*

77*

—; 1.61'

Carnivora; Procyonidae

Lemur catta

2100''

22.00*

1*

135*

—; 1.09'

Primates; Lemuridae

Dasyprocta aguti

2800*

20.30*

1.3*

104*

—; 0.83'

'Derived using the formulas or data of Bauchot and Stephan (1966) for the "index of progression" (IP) or Jerison (1973) for the "encephalization quotient" (EQ).

"Bauchot and Stephan (1966).

*Sacher and Staffeldt (1974).

'computed by this author.

/Pirlot and Stephan (1970).

Source-. Data arranged in approximate groupings of increasing size.

n"

r ft

Ol MO

strongly precocial mammals, and thus this has been a defining feature of our order from its very origins.

Encephalization and Precociality

The summaries presented in Table 3 indicate that one key component of the precocial reproductive strategy within mammals is relatively high encephal-ization (Martin, 1975a,b; 1982; Martin and MacLarnon, 1985). This makes sense in developmental, functional, and ecological terms. Precocial mammals are characterized by elongated gestation periods (Martin and MacLarnon, 1985), with their typically high rates of intrauterine brain growth (Sacher and Staffeldt, 1974). Large neonatal and adult relative brain size is a key component of an overall adaptive strategy based on low mortality, complex social organization, and high learning requirements (Dunbar, 1998). As noted, this adaptive configuration is likely linked to evolution in relatively stable tropical environments with predictable resource distributions, competition levels, and mortality schedules.

Martin (1981), and Martin and MacLarnon (1985) quantified the association of precociality in mammals and size-corrected estimates of brain size. There is a significant upward transposition or "grade shift" for precocial mammals versus altricial mammals (Martin, 1981). Figure 7 illustrates this schematically and gives Martin's (1981) regressions for the two groups of mammals. It seems that having relatively large brain size is a key component of reproductive and life history strategy in the precocial mammals. This is undoubtedly linked at least in part to the role of learning, and various cognitive and memory skills in species with prolonged growth, low reproductive turnover, and, in many cases, complex social organization (Dunbar, 1998; Kudo and Dunbar, 2001). There are of course other inputs to relative brain size that are likely operative in the case of particular groups that are precocial. Considering only two examples, the high encephalization of dolphins and some other cetaceans appears related to some extent to diving patterns and/or social complexity (see Marino 1996, 1997), while a significant component of primate encephalization may be due to cortical enlargement linked to visual processing (Preuss, this volume).

The association between precociality and high adult relative brain size is not absolute by any means. Various altricial mammals—particularly some of the carnivores—are also quite highly encephalized. In such species the brain grows considerably after birth. This pattern also characterizes our own

2 OD

... Precocial Altricial

Body size

Figure 7. A schematic representation of brain-body scaling in precocial versus altricial adult mammals, with regression values given for each group. Precocial species exhibit a significant upward transposition or "grade shift" relative to altricial species, as indicated by the higher value for the y-intercept parameter. Note that this effect is most strongly marked in smaller size ranges. See text for additional discussion (after Shea, 1987, and based on data from Martin and MacLarnon, 1985, 1988).

species, often described as "secondarily altricial" (Gould, 1976), although this aspect of human development obviously overlays typically strong anthropoid precociality. In birds, altricial species are generally more encephalized as adults than are precocial species (Ricklefs and Starck, 1998). These altricial birds merely exhibit higher duration and rates of postnatal brain growth.

Following Martin's (1981) claims regarding relative brain size and reproductive strategies in mammals, Bennet and Harvey (1985) stressed that these results emerged essentially from phylogenetic bias (i.e., having too many primates in the overall sample). They suggested that there is in fact no statistical difference in EQ values for precocial versus altricial mammals once such phy-logenetic factors are controlled. In order to more fully address this issue, we need to consider an additional key factor in these analyses. That factor is the role that body size may play in the broader context of reproductive strategies and encephalization.

Pregnancy And Childbirth

Pregnancy And Childbirth

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