Empirical and Theoretical Constraints on the Evolution of Lactation

V. HAYSSEN Department of Biological Sciences Smith College Northampton, MA 01063

ABSTRACT ment during gestation, so too, the age at For 829 mammalian species, data on first solid food may alter or reflect the age at weaning or age at first solid food rate of energetic investment during lacta- were analyzed with respect to body tion. Thus, the age at first solid food mass, phylogeny, habitat, diet, length of relative to the age at weaning may indi- gestation, basal metabolism, and neona- cate the function of lactation within the tal development. The primary influence reproductive biology of a given mam- on lactation length is female mass, but mal. Testing these hypotheses will re- phylogenetic constraints are important. quire data from diverse species on the Thus, lactation can be characterized as nutritional and energetic value of milk short (earless seals and baleen whales), before and after first solid food as well long (marsupials, bats, and primates), or as on the mechanics and consequences of average (remaining eutherians). Among nursing or suckling during the course of average , lagomorphs have lactation. short lactations. (Key words: evolution of lactation, al- Lactation may have different func- lometry, reproductive effort, parental in- tions, evolutionary constraints, and phys- vestment) iological control depending on whether Abbreviation key: BMR = basal metabolic young first eat solid food near weaning rate. or well before it. First solid food eaten near weaning occurs in polytocous spe- cies with altricial young; in this case, INTRODUCTION lactation has a clear energetic role. In Lactation is the quintessence of mammals. contrast, first solid food well before Like the evolution of mammals, the evolution weaning is common for mammals with of lactation has incorporated many organiza- single, precocial offspring. For these spe- tional changes. Biochemical changes involve cies, the energetic and nutritional con- carbohydrate, fat, and protein synthesis in the straints on lactation may be less impor- female and their catabolism in her young. tant than the benefits of maintaining Gland structure and location are anatomically contact between mother and young, such and developmentally modified in females, as as reduced juvenile mortality and in- are cheek musculature and tooth growth in creased opportunities for learning social young. Physiological changes include modifi- or foraging patterns. Thus, the age at cations not only of hormonal control and me- first solid food relative to the age at tabolism, but also of the behaviors of mothers weaning may indicate the function of and their young in order to implement and to lactation within the reproductive biology integrate nursing and suckling. Lactation alters of a given . the timing of reproduction to mesh ecologi- Delayed development and implanta- cally, energetic demands with seasonal re- tion alter the timing of energetic invest- source abundance. To achieve this organiza- tional integration, the genetic framework supporting lactation and other reproductive Received July 31, 1992. traits is likely to be replete with pleiotropy and Accepted November 23, 1992. polygeny. Thus, the selection pressures on lac-

1993 J Dairy Sci 76:3213-3233 3213 3214 HAYSSEN tation are, and have been, numerous and com- (lactation length) is available for 753 species, plex. and age at first solid food is available for 419 Most mammalian traits (e.g., body length, species. These and additional data on milk number of toes, and dentition) are characteris- composition, length of gestation (including di- tics of individuals, but lactation and other apause and implantation delays), development reproductive characteristics are not. In particu- at birth, litter size, and adult female mass were lar, the length of lactation is not determined synthesized from over 12,000 sources (1, 5, 7). solely by the mother or by the young but rather Common log transformations were performed depends on their interaction. Selection acts on on the age at weaning, age at first solid food, at least two genetic complements simultane- length of gestation, and adult female mass to ously. Reproductive characteristics, such as improve the symmetry of each distribution lactation, are characteristics of family groups, across species and the uniformity of spread not of individuals. The evolutionary processes across orders (8). Not all data were available that affect reproductive characteristics have not for each species. The age at first solid food is been delineated, but trait group or interdemic more precisely and uniformly defined than the (between populations) selection may be impor- age at weaning. Unfortunately, the age at first tant (11). The study and characterization of solid food is recorded about half as often. lactation solely on the molecular, cellular, or More observations of the age at first solid food individual level miss the essential character of are needed. this phenomenon. Operational definitions of the length of lac- This paper explores lactation across mam- tation (the age of weaning) vary according to malian species and assesses the relative impor- the needs of the investigator. Unless this varia- tance of diverse biological aspects (for exam- bility is correlated with a more natural aspect ple, habitat, diet, body mass, and phylogenetic of mammalian biology (for instance, body history) to the temporal and energetic charac- mass or phylogeny), subsequent analysis of teristics of lactation. Temporal aspects will be relationships, although not biased, will be emphasized because the energetic aspects (milk more difficult to elucidate. In some cases, the quality and quantity) have already received needs of investigators probably are confounded extensive analysis and, more importantly, be- with phylogeny (e.g., primatologists study pri- cause time itself is a limiting resource and a mates; the whaling industry studies whales). potent evolutionary pressure. Reproduction Unfortunately, the biases inherent in these must fit into a seasonal climatic cycle, where different approaches to mammalian groups such a cycle exists. Additionally, reproductive have not been precisely delineated. Thus, their success depends on the production of as many effect on comparative analyses are unknown. viable offspring as possible over a lifetime; the Several temporal units are used to record sooner that these offspring can be produced, the length of reproductive stages: days, weeks, the greater is the selective advantage (2). Time months, and years. As units, weeks and is essential for parents, for offspring, and for months have little biological relevance because populations during periods of exponential most species are unaware of our human meas- growth and in saturated environments. Thus, urement of time. Measurement of lactation and the duration of lactation is an important aspect other reproductive stages in these units is not of the reproductive biology of mammals. An biologically meaningful and should be additional advantage of this particular analysis avoided. The use of months as a unit is espe- is to provide the means to estimate the lacta- cially problematic because the measure cannot tion lengths of extinct, rare, or unstudied mam- be accurately rescaled into another time frame. mals based on maternal mass and phylogeny. A single month can range from 28 to 31 d. For this report, all temporal measures have been MATERIALS AND METHODS converted to days, and a month is assumed to be 30 d. Data on lactation lengths have been For this paper, lactation length is considered recorded for about one-fifth of the known to be a dependent variable, and description of mammals, representing 19 or 20 taxonomic its variance with respect to a variety of other orders. Of these 829 species, age at weaning variables is the major goal. Statistical treat-

Journal of Dairy Science Vol. 76, No. 10, 1993 SYMPOSIUM: LIMITS TO LACTATION 3215 ment was by least squares regression or analy- or first solid food and the common names of sis of covariance (5, 9). Least squares regres- representative species follow: infraclass Pro- sion was chosen over reduced major axis totheria, order Monotremata (3 species; echid- regression to maintain a constant dimensional- nas and platypus); infraclass Metatheria, order ity of slopes across different data sets. Statis- Marsupialia (89 species; opossums, phalangers, tics for significant regression analyses are kangaroos, wombats, and koala); infraclass Eu- reported. For each set of regressions, a sig- theria, orders Xenarthra or Edemata (9 species; nificance of .05 across sets was approximated anteaters and sloths), Insectivora (38 species; by reducing the significance for individual hedgehogs, shrews, and moles), Scandentia (3 regressions by the number of regressions per- species; tree shrews), Dermoptera (no data; fly- formed for that analysis. Thus, to be reported, ing lemur), Chiroptera (75 species; bats), Pri- individual regressions for analysis by in- mates (64 species; lemurs, monkeys, apes, and fraclass needed P < .0167 (.05/3 infraclasses), humans), Carnivora (128 species; wolves, whereas ordinal comparisons needed P < .0025 bears, raccoons, weasels, genets, mongooses, (.05/20 orders), and familial regressions needed hyena, cats, fur seals, walrus, and earless P < .0004 (.05/136 families). seals), Cetacea (28 species; dolphins, por- Several dimensionless ratios were calcu- poises, and whales), Sirenia (3 species; dugong lated to explore mammalian lactation. Al- and manatees), Proboscidea (2 species; though they are not amenable to rigorous para- elephants), Perissodactyla (9 species; zebras, metric analysis, these ratios, nevertheless, are tapirs, and rhinoceroses), Hyracoidea (3 spe- extremely useful for illustrating multidimen- cies; hyraxes), Tubulidentata (1 species; aard- sional trends. The ratio of age at first solid vark), Artiodactyla (82 species; swine, camels, food to age at weaning may be an estimate of hippopotamus, deer, giraffe, cattle, antelope, the relative nutritional dependency of the off- sheep, and goats), Pholidota (3 species; pango- spring on lactation. The ratio of lactation lins), Rodentia (270 species; , gophers, length to the period between conception and kangaroo rats, beaver, voles, hamsters, gerbils, weaning (gestation plus lactation) is an esti- mice, rats, and ), Lagomorpha (15 mate of the relative contribution of lactation to species; pikas, hares, and rabbits), and Macro- a female’s temporal investment in reproduc- scelidea (4 species; elephant shrews). The in- tion. Although the energetic costs of construc- fraclasses Metatheria and are referred tion and maintenance of placental structures to jointly as the taxon Theria. The Appendix are not included, the ratio of litter mass at birth provides selected familial common names. to female mass is an estimate of the energetic investment into a given reproductive effort be- RESULTS AND DISCUSSION fore lactation begins. Similarly, the ratio of an individual neonate’s mass to maternal mass is Univariate Statistics an estimate of the energetic investment into a single offspring before lactation begins and an Age at Weaning. The length of lactation in estimate of the reliance on lactation for the mammals (Figure 1) ranges almost three orders physical growth of an individual offspring. Of of magnitude, from 4 to 5 d in hooded seals course, for single litters, litter mass and neona- (Cystophora cristata, family Phocidae, order tal mass are identical. Carnivora), spiny rats (Proechimys guairae, family Echimyidae, order Rodentia), and ele- Taxonomic Representation phant shrews (Macroscelides proboscideus, fa- mily Macroscelididae, order Macroscelidea) to The ordinal representation of the species in over 900 d in some of the great apes (chimpan- this data set is roughly similar to that for zees, Pan troglodytes, and orangutan, Pongo mammals. Small mammals (Insectivora, pygmaeus, family Pongidae, order Primates). Chiroptera, and Rodentia) are underrepresented Although extremely short lactation lengths by 5 to 10%, whereas marsupials, primates, (<10 d) are rare, long lactation lengths (>500 d) and carnivores are overrepresented by similar are common for large-bodied species with sin- amounts. For each mammalian order, the num- gleton offspring, such as kangaroos, great apes, ber of species with data on the age at weaning walruses, whales, sirenians, elephants, and

Journal of Dairy Science. Vol. 76, No. 10, 1993 3216 HAYSSEN rhinoceroses. Overall, 50% of known lactation eaten within wk 1 after birth (occasionally on lengths range from 29 to 135 d. The median the day of birth) in hystricomorph , lactation length is 60 d, the geometric mean is such as guinea pigs, porcupines, coypus, and 64.56 d (1.81 log10 d, SD = .428), and the , as well as in other mammals, such as arithmetic mean is 108.4 d (SD = 132.1). The sloths, zebras, hyraxes, and bovids. In contrast, peak at about 30 d may be an artifact of using first solid food is nearly coincident with wean- human-biased units such as weeks or months ing in many sciurid (e.g., squirrels) and muroid rather than more biologically meaningful units (e.g., rats or gerbils) rodents and may even such as days. occur after weaning, as with earless seals. Age Generally, lactation lengths for prototheri- at first solid food ranges from 1 to 300 d; 50% ans (monotremes) and metatherians (marsupi- of the observations are from 14 to 50 d. The als) are longer than those for eutherians (me- median age is 30 d, the geometric mean is dian lactation length: prototherians, 150 d, 3 27.54 d (1.44 log10 d, SD = .455), and the species; metatherians, 120 d, 75 species; eu- arithmetic mean is 45.1 d (SD = 50.9). The therians, 50 d, 675 species), although lactation median age at first solid food is later for lengths are longest in eutherians. Lactation in metatherians (75 d, 72 species) than for eu- monotremes and marsupials, but not eutheri- therians (22 d, 345 species). Sufficient data on ans, encompasses the exponential period of first solid food for prototherians are lacking. offspring growth. Additionally, lactation in Comparisons and Analysis. For both age at marsupials is distinctly biphasic. During the weaning and age at first solid food, the median phase of continuous teat attachment, marsupial and the geometric mean are within 10% of milk is high in carbohydrates and low in lipids, each other, but the arithmetic mean is at least whereas the reverse holds when suckling is 50% larger. Thus, the log10-transformed data intermittent (3, 10). Occasionally, the teat at- more closely approximate Gaussian distribu- tachment phase of marsupial lactation is tions for both variables. equated with the chorioallantoic phase of eu- The interquartile range of the age at first therian gestation. Superficial similarities exist, solid food (36 d, 419 species) is about a third but this synonomy ignores the vastly different that of the age at weaning (106 d, 753 species). proximate mechanisms (metabolic and physio- The smaller sample size for age at first solid logical control) and ultimate causes (selective food may account for its smaller range, or the pressures and evolutionary constraints) that age at first solid food may be less flexible and distinguish gestation and lactation from each more uniform across mammals than the age at other. weaning. Age at First Solid Food. Fewer data exist Age at weaning and age at first solid food for the age at first solid food. Solid food is are positively correlated (regression statistics: r = .58; R2 = .34; F = 176; sample size, 343 species). Species that are older at weaning are also older at first solid food. Age at weaning and age at first solid food are both positively correlated with female mass, although the ef- fect is weak for age at first solid food (see Table 1, Equation [1] for age at weaning statis- tics; regression statistics age at first solid food: r = .19; R2 = .03; F = 15; sample size, 408 species). Analysis of the ratio of age at first solid food to age at weaning effectively removes the confounding influence of body mass. In general, the longer the lactation length, the sooner first solid food occurs relative to wean- Figure 1. Frequency of lactation lengths in 753 species ing. For eutherians with lactation lengths of at of mammals. The peak at 30 d may be an artifact of the use of anthropocentric units (e.g., weeks or months) rather least 1 yr (21 species), most (90%) have an age than biologically meaningful units (e.g.. days). at first solid food within the first third of the

Journal of Dairy Science Vol. 76, No. 10, 1993 SYMPOSIUM: LIMITS TO LACTATION 3217 lactation period. For 62% of these species, food and activity. Both groups (especially the solid food is eaten within the first fifth of baleen whales) exert great statistical influence lactation. In contrast, for eutherians with lacta- on the computed relationship between lactation tion lengths <50 d (123 species), few (11%) length and body mass. Removal of these two have an age at first solid food within the first groups from the calculations generates a more third of lactation. For 48% of these species, representative numerical relationship for mam- first solid food occurs during the last third of mals in general (Table 1, Equation [2]). lactation. Thus, infants depend completely on The remaining mammals are still not a maternal resources for a larger proportion of homogeneous group, because several mam- the lactation period in species with short lacta- malian taxa have distinctly long lactation tions, whereas offspring may be less reliant on lengths for their mass. Bats, primates, and maternal nutrients when lactation lengths are marsupials together form a homogeneous long. The timing of first solid food relative to group of mammals with lactation lengths weaning is also correlated with litter size and longer than those of other mammals with simi- with neonatal development as described more lar maternal mass. Covariance analysis con- fully later. firms this observation (Table 1, Equations [3] and [4]). The slopes of the two regression lines Allometry of Lactation: The Relationship are not statistically distinguishable; thus, the of Lactation to Maternal Mass relationship between lactation length and body mass is not different between the two groups. For mammals, the length of lactation is However, the intercepts of the equations are positively correlated with adult female mass different. Bats, marsupials, and primates, as a (Figure 2; Table 1, Equation [1]). In general, group, have lactation lengths 50% longer (on a larger species have longer lactation lengths, log10 scale) than other therians of comparable although several interesting exceptions to this masses. The Prototheria (monotremes) are in- pattern exist. termediate. Although the reproductive biology Earless seals (family Phocidae) and baleen of marsupials is generally different than that of whales (infraorder Mysticeti), but not other eutherians (6), marsupials are indistinguishable marine mammals, have much shorter lactation from bats and primates with respect to lacta- lengths than expected for their body masses. tion length. Thus, for lactation length, in- The extremely short lactation lengths of earless fraclass comparisons are not appropriate. seals appear to be related to the unpredictable Why should mammals with long and aver- and short existence of the ice floes where they age lactation lengths have similar allometric breed. The relatively short lactation lengths of relationships? One explanation is that the baleen whales may reflect the timing of their similarity of slope between long and average annual migrations, because a lactation length mammals is accidental. In other words, bats, appropriate to their large mass would not be marsupials, and primates each have a separate, synchronized with the seasonal nature of their selective advantage for long periods of lacta-

TABLE 1. Allometric relationships between the age at weaning (days) and adult female mass (grams) for various mammalian groups.1 Slope SE Constant SE R2 n F Mammalia .184 .008 1.275 .026 .43 732 543 Mammalia2 (no short) .214 .008 1.212 .025 .51 705 743 Long lactations3 .227 .012 1.501 .033 .62 201 329 Average lactation4 .250 .006 .977 .021 .75 504 1517

1 All variables are log10-transformed. Sample size is number of species. 2Therian mammals without earless seals (Phocidae), baleen whales (Mysticeti). 3Includes marsupials (Marsupialia), primates (Primates), and bats (Chiroptera) only. 4Eutherians, excluding primates (Primates), bats (Chiroptera), earless seals (Phocidae), and baleen whales (Mysticeti).

Journal of Dairy Science Vol. 76, No. 10, 1993 3218 HAYSSEN tion, but, because the three taxa are adjacent neonatal marsupials are physically. Compara- and slightly overlapping with respect to body tive data on the developmental similarities of mass, they form a single group with the same marsupials, bats, and primates and on the qual- slope as that for other mammals. However, if ity and quantity of milk over the course of the slope is regarded as a true biological lactation in these groups, especially bats, are phenomenon (i.e., that an ancestral allometry needed to explore this empirical relationship. of mass with lactation length exists for mam- Thus, mammalian lactation lengths relative mals), then the convergence of marsupials, to maternal mass can be characterized as short bats, and primates needs explanation. (earless seals and baleen whales), long (marsu- Given the fetal state of their neonates, the pials, bats, and primates), or average (the re- relatively long lactation lengths of metatheri- maining eutherians). For this last (average) ans (marsupials) are not surprising; however, group, 75% of the variation in the length of neither bats nor primates have such tiny off- lactation is related to maternal mass. The spring relative to maternal mass. Some meta- correlation of lactation length with body mass bolic parameter or growth rate may possibly is stronger for larger species (>1 kg vs. <=1 kg), explain the allometric convergence. The but this result is confounded by phylogeny, lengthy primate lactations may be related to because about 75% of the small mammals with the more extensive psychosocial growth and average lactation lengths are rodents. development characteristic of the order. A Eutherian Ordinal Analyses. Although lac- similar developmental phenomenon may occur tation is strongly correlated with maternal in bats that is related to the extensive neu- mass across mammalian species, within in- romuscular coordination required for food ac- dividual eutherian orders, the relationship be- quisition in flight. Perhaps newborn bats and tween female mass and lactation length is less primates are as “fetal” in their neurological obvious (Figure 3). Many systematically dis- development relative to their adult needs as tinctive orders (tree shrews, sirenians,

Figure 2. Allometric relationship of lactation length with female mass (732 species). Marsupials, bats, and primates form a homogenous group with long lactations. Baleen whales and earless seals have unusually short lactations. Key to orders: infraclass Prototheria; order Monotremata (P), infraclass Metatheria, order Marsupialia (+); infraclass Eutheria, orders Artiodactyla (A), Chiroptera (B), Carnivora (C), Proboscidea (E), Pholidota (F), Hyracoidea (H), Insectivora (I), Scandentia (K), Lagomorpha (L), Primates (M), Rodentia (R), Sirenia (S), Tubulidentata (T), Cetacea (W), Xenarthra (X), Macroscelidea (Y), and Perissodactyla (Z). Common names are given in Materials and Methods.

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Figure 3. Box plots of lactation length (log10-transformed age at weaning in d) for 753 mammalian species grouped by order and ranked by median maternal mass (provided beneath name of order). Sample size in number of species is listed in the right column. Lagomorphs have relatively uniform and short lactations. Carnivore lactation lengths have the broadest range. Median (+), interquartile range ( • ), approximate 95% confidence interval for median ( ), outliers, the values distant from the median by >1.5 times the interquartile range (*), and “whiskers”, the range excluding outliers (—). Names of common representatives of each order are given in Materials and Methods.

Journal of Dairy Science Vol. 76, No. 10, 1993 3220 HAYSSEN elephants, hyraxes, aardvarks, pangolins, and The six families of the order Insectivora elephant shrews) have too few species for anal- (which includes hedgehogs, tenrecs, shrews, ysis. For others, such as xenarthrans, peris- moles, etc.) are a taxonomic mixture with little sodactyls, and lagomorphs, the absence of a close phylogenetic relationship. Data for 36 of statistical relationship between lactation length the 379 species (10%) are available. Maternal and female mass may be an artifact of the mass varies over almost three orders of magni- narrow range of body masses present across tude, but lactation lengths are nearly all be- species within these orders. However, the tween 20 and 50 d (median 28 d). Thus, within range of body masses in each of several other this order, the duration of lactation and female orders (insectivores, bats, carnivores, and ceta- mass are not correlated (Figure 4b). However, ceans) spans three to four orders of magnitude; phylogeny confounds this analysis: shrews however, for these groups, lactation length also (family Soricidae) tend to be small; moles is not correlated with maternal mass. Only for (family Talpidae) are larger; tenrecs (family primates, artiodactyls, and rodents is lactation significantly related to maternal mass, and only Tenrecidae) are intermediate; and hedgehogs for primates and artiodactyls does body mass (family Erinaceidae) are often the largest. Al- explain >50% of the variance in lactation though Insectivora generally have lactations of length (Table 2). For eutherian orders average duration for mammals of their mass, represented in the data set by at least 3 fami- the small soricids (shrews <10 g) tend to have lies or 15 species, descriptions of the allometry longer lactation lengths than expected. of lactation length follow (Figures 4 to 7). With at least 17 families, 175 genera, and The four families of xenarthrans (which in- over 900 species, bats (order Chiroptera) are cludes anteaters, two- and three-toed sloths, second only to rodents in phylogenetic diver- and armadillos) are each remnants of previ- sity. Unfortunately, data on lactation are avail- ously diverse taxa. Data for 6 of the 29 species able for only 8% of the species (representing (21%) are available. Although lactation lengths 37 genera and 10 families). For 85% of these are highly varied among species with similar limited observations, lactation length is be- female mass (Figure 4a), overall, they are near tween 30 and 90 d. Maternal mass spans nearly those expected for average mammals of three orders of magnitude but accounts for equivalent size. only 8% of the variation in the length of

TABLE 2. Regression statistics for significant allometric relationships between the age at weaning (days) and adult female mass (grams) for various mammalian taxa.1 Slope SE Constant SE R2 n F Infraclass Metatheria .197 .017 1.628 .047 .64 74 129 Eutheria .191 .008 1.210 .026 .48 655 608 Order Marsupialia .197 .017 1.628 .047 .64 74 129 Primates .334 .043 1.104 .148 .51 59 61 Artiodactyla .271 .032 .831 .154 .51 69 73 Rodentia .150 .015 1.153 .032 .30 242 103 Fissipedia2 .180 .026 1.238 .098 .36 85 49 Family Dasyuridae .137 .020 1.771 .038 .64 27 46 Macropodidae .340 .038 1.172 .141 .85 15 82 Mustelidae .168 .031 1.314 .100 .53 25 28 Bovidae .237 .040 1.001 .195 .45 42 34 1For each set of regressions, a significance level of .05 was approximated by reducing the significance for individual regressions by the number of regressions performed for that analysis: infraclass regressions (P < .0167); ordinal regressions (P < .0025); and familial regressions (P < .0004). Sample size is number of species. All variables are log10- transformed. 2Carnivora, excluding the Pinnipedia (Otariidae, Odobenidae, Phocidae).

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Figure 4. Allometric relationships of age at weaning with maternal mass for a) edentates, b) insectivores, and c) bats. Species from the same family have the same letter code. Key to families within each order: a. Edentata or Xenarthra: Bradypodidae (B), Choloepidae (C), Dasypodidae (D), and Myrmecophagidae (M): b. Insectivora: Chrysochloridae (C), Erinaceidae (E), Tenrecidae (N), Solenodontidae (O), Soricidae (S), and Talpidae (T); c. Chiroptera: Emballonuridae (E), Phyllostomidae (F), Megadermatidae (G), Rhinolophidae (L), Molossidae (M), Noctilionidae (N), Pteropodidae (P), Rhinopomatidae (R), Vespertilionidae (V), and Nycteridae (Y). Familial common names are given in the Appendix.

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Figure 5. Allometric relationships of age at weaning with maternal mass for a) primates, b) carnivores, and c) Cetaceans. Species from the same family have the same letter code. Key to families within each order: a. Primates: Cebidae (B), Cercopithecidae (C), Daubentoniidae (D), Galigonidae (G), Hominidae (H), Indridae (I), Cheirogaleidae (K), Lemuridae (L), Callimiconidae (M), Lorisidae (O), Pongidae (P), and Callitrichidae (Y); b. Carnivora: Protelidae (A), Canidae (C), Felidae (F), Herpestidae (H), Mustelidae (M), Otariidae (O), Procyonidae (P), Phocidae (S), Ursidae (U), Viverridae (V), Odobenidae (W), and Hyaenidae (Y); c. Cetacea: Balaenopteridae (B), Delphinidae (D), Eschrichtidae (E), Monodontidae (M), Phocoenidae (P), Platanistidae (R), Physeteridae (S), and Ziphiidae (Z). Familial common names are given in the Appendix.

Journal of Dairy Science Vol. 76, No. 10, 1993 SYMPOSIUM: LIMITS TO LACTATION 3223 lactation (Figure 4c). Insectivora and Chirop- dimensional environment, and their longer lac- tera have a similar range of female mass, and tation lengths may reflect this developmental both orders exhibit little correlation of body constraint. Clearly, more precise data are mass with lactation length; however, the me- needed to confirm the unusual negative corre- dian lactation length for bats (60 d) is over lation of lactation and body mass in cetaceans. twice that of the Insectivora (28 d). Like the xenarthrans, the three families of Primates also lactate for long periods rela- perissodactyls (which include zebras, tapirs, tive to most mammals. Maternal mass is and rhinoceroses) are remnants from previ- strongly and positively correlated with lacta- ously more diverse taxa. Lactation data are tion length (Figure 5a) and accounts for >50% available for 9 of 18 species (50%). The larger of the variation in the length of lactation (Table rhinoceroses have the longest lactation lengths, 2). Although the ordinal trend (based on 33% but, overall, the duration of milk production is of the known species) is clear, no strong corre- only weakly correlated with female mass lation between mass and lactation length exists (Figure 6a). within any primate family. In contrast, over 50% of the variation in Of mammalian orders with >20 species, lactation length is correlated with maternal carnivores and artiodactyls are the best known. mass for artiodactyls (which include pigs, pec- Each has lactation length data recorded for caries, camels, hippopotamuses, deer, giraffes, 43% of its species. The increasing variance in and antelope; Figure 6b; Table 2). Bovids lactation length with body mass in carnivores (antelope, cattle, sheep, and goats) constitute is distinctive. Nearly all female carnivores <10 60% of the artiodactyla data set, and lactation kg lactate from 30 to 130 d. However, of those lengths of bovids are strongly and positively carnivores >10 kg, some ursids (bears), most correlated with maternal mass (Table 2). otarids (fur seals), and odobenids (walruses) Lagomorphs come in three sizes (100- to have lactation lengths >130 d, whereas many 500-g pikas, 500- to 1500-g rabbits, and phocids (earless seals) wean their young <30 d 2- to 3-kg hares), but lactation ranges only after birth. Exclusion of the pinnipeds im- between 17 and 28 d for the entire order, proves the homoscedasticity and generates a represented by 15 of 62 species (24%). Not significant allometric equation (Fissipedia, Ta- only do lagomorphs tend to have relatively ble 2). Lactation lengths for mustelids (e.g., invariant periods of lactation, they also have weasels, skunks, and badgers) are strongly and short lactation lengths compared with other positively correlated with maternal mass (Table mammals of similar mass (Figure 7a). The 2), and the few data for procyonids (raccoons) leporids (hares and rabbits) have neonates and viverrids (genets) also suggest a positive widely divergent in developmental condition at correlation with female mass. For the remain- birth; the larger hares produce precocial young, ing carnivore families, lactation length appears whereas the smaller rabbits produce altricial to be relatively independent of maternal mass young. Perhaps as a result, first solid food is (Figure 5b). about 1 wk earlier for precocial hares than for Few of the data on cetacean lactation altricial rabbits. Hares have shorter lactations lengths are from direct observations of live than expected given their mass, but whether mother and calf pairs over the course of lacta- this difference is due to the production of tion. Most data are estimates from the seasonal precocial young or to a general trend toward presence of milk in adult females and in calves short lactation lengths within lagomorphs is killed by the commercial whaling industry. not clear. Delineation of the differences be- These data represent 36% of the known species tween hares and rabbits in the physiology and and suggest that the large baleen whales lactate ecology of lactation could be especially useful for shorter periods than the smaller toothed because the two groups are both polytocous, whales. Because smaller cetaceans have lacta- they have similar diets and phylogenetic ances- tion lengths more in keeping with their body try, and they can have sympatric populations mass, the overall trend is an inverse relation- (i.e., they coexist in the same location). Thus, ship of lactation with body mass (Figure 5c). the two groups form a natural control for the Like bats, toothed whales must catch in- effects of diet, habitat, and phylogeny on the dividual food items in a dynamic, three- production of altricial versus precocial young.

Journal of Dairy Science Vol. 76, No. 10, 1993 3224 HAYSSEN Rodents are the largest mammalian order, Reproductive Effort and the Length of Lactation and lactation data are available for about 15% Temporal Investment. Time and energy are of the >1700 species. Maternal mass ranges two components of maternal investment. Mam- from 6 g to 35 kg, but almost 90% of the mals can dissociate the temporal and energetic lactation lengths are between 10 and 50 d, and components of reproductive investment during half are between 21 and 38 d (Figure 7b). gestation, through diapause and delayed im- Thus, for rodents, lactation is only modestly plantation, and during lactation, via early first correlated with maternal mass (Table 2). solid food and altered milk composition or Sciurid (e.g., squirrels) rodents have long lacta- production. Although the energetic demands of tion lengths relative to maternal mass. a current reproduction effort clearly affect fu- Cricetids (e.g., hamsters, gerbils, and deermice) ture reproductive success, temporal aspects are may have shorter lactation lengths than murids also important, especially in temperate or other (e.g., rats and house mice) of similar size, climatically seasonal environments. Appropri- although the overlap between them is large. ate timing of the energetic demands of

Figure 6. Allometric relationships of age at weaning with maternal mass for a) odd-toed ungulates (perissodactyls) and b) even-toed ungulates (artiodactyls). Species from the same family have the same letter code. Key to families within each order: a. Perissodactyla: Equidae (E), Rhinocerotidae (R), and Tapiridae (T); b. Artiodactyla: Bovidae (B), Camelidae (C), Cervidae (D), Giraffidae (G), Hippopotamidae (H), Tragulidae (M), Suidae (S), and Tayassuidae (T). Familial common names are given in the Appendix.

Journal of Dairy Science Vol. 76, No. 10, 1993 SYMPOSIUM: LIMITS TO LACTATION 3225 reproduction to coincide with periods of re- importance of females and offspring in the source abundance and environmental suitabil- evolution of a particular reproductive pattern. ity increases reproductive success. The length A female’s investment in her offspring be- of lactation is determined by the timing of gins at conception; thus, lactation is only one weaning. Yet, mothers and their offspring may component of reproductive effort, and the tim- be in conflict regarding the timing of weaning ing of weaning depends, in part, on the length relative to the seasonality of resource abun- of gestation. Marsupials may spend >90% of dance. The energetic demands on females the period between conception and weaning on usually are largest before weaning, but the lactation, and phocid seals may devote <5% of period after weaning is the most demanding their temporal investment on lactation, but for offspring. The length of lactation and the these groups are exceptional (Figure 8). Given timing of weaning may reflect the relative that mammalian gestation and lactation lengths

Figure 7. Allometric relationships of age at weaning with maternal mass for a) pikas, hares, and rabbits (lagomorphs) and b) rodents. Species from the same family have the same symbol or letter. Key to families within each order: a. Lagomorpha: Leporidae (L) and Ochotonidae (O); b. Rodentia: Muridae (+), Sciuridae (o), Cricetidae (x), Arvicolidae (A), Bathyergidae (B), (C), Dasyproctidae (D), Echmyidae (E), Agoutidae (F), Gliridae (G), Hystricidae (H), Erethizontidae (I), (J), Heteromyidae (K), Aplodontidae (L), Myocastoridae (M), Octodontidae (O), Pedetidae (P), Hydrochaeridae (Q), Rhizomyidae (R), Spalacidae (S), Thryonomyidae (T), Capromyidae (U), (V), Chinchilli- dae (Y), and Zapodidae (Z). Familial common names are given in the Appendix.

Journal of Dairy Science Vol. 76, No. 10, 1993 3226 HAYSSEN

Figure 8. Box plots of the proportion of the period from conception to weaning, which is lactation for 653 mammalian species grouped by order and ranked by median gestation length (provided beneath name of order). Sample size in number of species is listed in the right column. For most eutherians, lactation occupies about half of the period between conception and weaning. For most prototherians and metatherians, lactation is usually over 75% of the parental investment period. Median (+), interquartile range ( • ), approximate 95% confidence interval for median ( ), outliers, the values distant from the median by >1.5 times the interquartile range (*), and “whiskers”, the range excluding outliers (—). Names of common representatives of each order are given in Materials and Methods.

Journal of Dairy Science Vol. 76, No. 10, 1993 SYMPOSIUM: LIMITS TO LACTATION 3227 range over nearly three orders of magnitude, temporal and energetic demands of lactation the percentage of time that a female spends in are different for the two mammalian groups lactation relative to the total period of with the shortest relative lactation lengths. reproductive investment is surprisingly con- Although a trade-off between gestation and stant across mammals. Generally, lactation oc- lactation might be expected, such that long cupies about half of the period between con- periods of lactation would compensate for ception and weaning (X = 49%; SD = 17%; short periods of gestation and vice versa, this median 48%, 653 species). Approximately trend is valid only for marsupials and earless 50% of these species have lactation lengths seals. For most mammals, after the effects of between 40 and 60% of the time between female mass are removed, the lengths of gesta- conception and weaning (lower quartile, tion and lactation are positively, not inversely, 39.3%; upper quartile, 57.3%). Thus, most correlated, although the effect is not strong mammals spend approximately the same (Table 3). Thus, mammals with long gestation amount of time in gestation as in lactation. lengths tend to have long periods of lactation, One practical consequence is that the gestation and mammals with short in utero development length of a mammal is a rough estimate of its tend to wean their offspring early. lactation length. Energetic Investment at Birth. The timing Mammals with extremely long or short lac- of first solid food relative to weaning may tation lengths do not have consistent patterns indicate the extent to which lactation is impor- of temporal investment. Marsupials have long tant to the nutritional or energetic needs of the lactation lengths, and for them lactation is a offspring. Thus, the timing of first solid food large percentage (75 to 95%) of the period relative to weaning may be of greater biologi- from conception to weaning. However, bats cal interest in the study of lactation than the and primates also have long lactation lengths, absolute age at either weaning or first solid but lactation for these groups is not an extraor- food. When the age at first solid food occurs dinary proportion of the time between concep- long before weaning, lactation may have sig- tion and weaning. Lactation lengths of bats, nificant functions beyond nutrition or energy. although relatively long for their mass, are The relationship of relative nutritional de- relatively short, <40% of their total parental pendency (age at first solid food divided by investment with none >65%. However, lacta- age at weaning) to the relative mass of off- tion lengths of most primates are about 40 to spring at birth (litter mass divided by female 60% of parental investment, and for about 10 mass) can be examined either with respect to species lactation is >65% of the period be- litter size (Figure 9a) or neonatal development tween conception and weaning. (Figure 9b). A clear pattern emerges, even Mammals with short lactation lengths are though neonatal development and litter size are similarly diverse. Earless seals have short lac- confounded. (Monotocous eutherians usually tation lengths (4 to 40 d), and lactation is also a have precocial young, whereas polytocous spe- small temporal component of their reproduc- cies often have altricial or semi-altricial neo- tive investment (gestation lasts about 1 yr). nates.) Similarly, baleen whales have short lactation lengths for their mass (.5 to 1 yr), but the contribution of lactation to the period between conception and weaning in these mammals is TABLE 3. Statistics for the multiple regression of body mass (grams) and the length of gestation (days) on the not relatively small; gestation lasts .8 to 1.2 yr l or about the same length as that of earless length of lactation (days). seals. Although the data are limited, milk com- Variable Coefficient SE position also appears to be similar between the Constant .911 .057 two groups. Milks from both groups are high Log female mass .122 .012 in fat and protein. In contrast, the age at first Log gestation .295 .040 solid food is probably very different. Earless 1For 634 species, after the effects of female mass are seals first ingest solid food after lactation is removed gestation and lactation lengths are positively over, whereas baleen whale calves probably 2 correlated (R = .47; F = 285). All variables are log10- first ingest krill well before weaning. Thus, the transformed.

Journal of Dairy Science Vol. 76, No. 10, 1993 3228 Hayssen

Figure 9. Relative nutritional dependency (age at first solid food divided by age at weaning) versus relative energetic investment at birth (litter mass at birth divided by maternal mass) broken down by a) litter size (litter sizes of 8 or more are coded as 8; 280 species) for all mammals or b) developmental state at birth for eutherians (70 species). Key to developmental state: altricial (1), semi-altricial (2). semi-precocial (3). and precocial (4). Single, precocial young are a smaller proportion of maternal mass at birth and rely less on lactation for nutritional support than the altricial young of polytocous species.

Journal of Dairy Science Vol. 76, No. 10, 1993 SYMPOSIUM: LIMITS TO LACTATION 3229 Monotocous, precocial eutherians have rela- spring growth and development via main- tively small offspring at birth (small percentage tenance of the parent and offspring bond. Sub- of adult mass), and these offspring eat solid sequent benefits include predator defense, food early in lactation. The young are furred, educational opportunity, and social facilitation. mobile, and complete in sensory function (eyes Predators may be less apt to attack a small and ears open) soon after birth, but they remain juvenile if a large adult is nearby, because that with their mothers for long periods. For these adult may directly intervene to protect the species, concurrent gestation and lactation sel- juvenile. Extended parental care can also pro- dom occurs. Overall, the relationship among vide an opportunity for young to learn from these reproductive characteristics—early first their parents about the location and quality of solid food, precocial singleton young, and food, nest sites, or potential threats. Finally, small relative mass at birth—is distinctive and few mammals with single precocial young are may be a highly derived condition. solitary. Most are born into a larger social Conversely, polytocous species with altri- arena of colony, troop, tribe, or herd. The cial or semi-altricial young are far more varia- survival and reproductive success of these ble. Litter mass can be a small or large propor- mammals depends on their integration into tion of female mass, and age at first solid food appropriate social roles. Long lactations that can occur early or late in lactation but usually continue after nutritional or energetic needs are occurs closer to weaning. In addition, gestation met facilitate this social integration. and lactation are commonly concurrent. The Differences in the energetic demands, production of multiple offspring with a large evolutionary constraints, and functional role of litter mass at birth, altricial development, and lactation between altricial, polytocous species late first solid food may be the ancestral eu- that have late first solid food and precocial, therian condition. monotocous species that have early first solid The consequences of each constellation of food suggest additional differences in the con- reproductive characteristics are varied. The lit- trol of lactation, its resistance to environmental ter mass at weaning of muroid rodents (altricial change, and the composition and output of litters with late first solid food) is often larger milk over time. For example, the frequency of than that of the mother, whereas a calf or a suckling and the duration of lactation may be human infant at weaning (single precocial off- under maternal control in polytocous species spring with early first solid food) is only a with late first solid food, whereas offspring are small fraction of maternal mass. In addition, more apt to control nursing and weaning when the mouse and vole weanlings have relied al- solid food is ingested early in lactation. The most entirely on their mothers for nutrients and cost to a mother of continuing to nurse a single energy during lactation, whereas the human offspring a fraction of her size that already infant and the calf supplement their diets with obtains a proportion of its nutritional require- solid food for a large portion of lactation. Not ments on its own is much less than that as- only are the demands of lactation enormous sociated with nursing multiple young that col- when multiple young are dependent for all lectively weigh as much or more than she their nutritional and energetic needs on milk, does. Thus, the cost to benefit ratios associated as with mice and voles, but, with concurrent with weaning are different. gestation, the female may also be meeting the Although lactation often extends or delays nutritional needs of a second, in utero, litter. gestation when the two are simultaneous, the Such a mother’s energetic budget and potential duration of lactation is also determined by for future reproductive success might be gestation, because the birth of a subsequent tightly constrained. litter forces the weaning of the first. Not only For species with single precocial offspring, are successive litters in conflict regarding the lactation may play a far different role in the timing of weaning, but littermates compete allocation of temporal and energetic resources throughout lactation for current maternal than it does in polytocous species with altricial resources. Maternal control over milk compo- young. Milk production may not be the pri- sition and production over the course of lacta- mary function of lactation; instead, selective tion allows females to fine tune their energetic pressures may operate on other aspects of off- investment as environmental conditions vary.

Journal of Dairy Science Vol. 76, No. 10, 1993 3230 HAYSSEN The composition of milk over the course of TABLE 4. Analysis of the variance in lactation length (380 species) with habitat and diet when broadly defined habitat lactation may be more closely tied to the needs 1 of the offspring when milk is the sole source and diet have little influence on the length of lactation. of energy and nutrients than when milk supple- Cumulative ments metabolic intake. In sum, maternal con- Independent variable F df R2 trol over the timing of weaning and the alloca- tion of metabolic resources may reduce Adult mass 595.93 1 .45 Infraclass 96.91 2 .59 intralitter and interlitter competition and, thus, Order (infraclass) 13.58 13 .72 allow a more selectively advantageous distri- Habitat 1.85 5 .73 bution across current and future reproductive Diet 2.19 2 .73 investment. 1 For further details, see the study by Hayssen (4). Lactation may be under tighter genetic con- trol (lower heritability) in species for which age at first solid food occurs close to weaning rather than close to birth because heritabilities are small for traits of critical importance to volant and marine) as well as specific diets reproductive fitness, and appropriate allocation (e.g., herbivores and carnivores); thus, habitat of resources during reproduction is more criti- and diet analyses are confounded with cal to survival and to reproductive success for phylogeny. The effects of habitat or diet on polytocous species with ingestion of solid food lactation may be more apparent within orders late in lactation. Thus, lactation may be less or families rather than across higher responsive to current offspring demands in phylogenetic categories. Such detailed analysis species for which age at first solid food is near is outside the realm of this review. Overall, for weaning. Responses to changing environmen- mammals, body mass and phylogenetic ances- tal conditions may be more important to fitness try have greater influence on lactation length in these mammals. Lactation may be most tied than do current habitat and diet. to the survival of current offspring in monoto- Milk Composition. When the primary role of lactation is social or protective, milk cous species with precocial young through the production and composition may be less cor- physiological regulation of gestation (including related with the long-term nutritional needs of the timing of birth) and the flexibility of its the offspring than with support of immediate genetic program across species. energetic demands. Thus, the low fat and pro- To test these hypotheses, data on the nutri- tein and the high sugar content of primate and tional and energetic value of milk before and ungulate milks may reflect the alternative after first solid food and data on suckling functions of lactation in these mammals. frequency, duration, initiation, and biochemical Milk may have a thermoregulatory function consequences over lactation and in a variety of for some mammals. Certainly, the high fat environmental conditions are needed for an composition of cetacean milk serves a ther- array of species. The captive breeding popula- moregulatory function in the offspring. More tions of diverse mammals in various zoos, direct thermoregulatory advantages may also especially those near research institutions that accrue. Many altricial offspring are unable to can analyze milk composition, provide an op- maintain high body temperatures, and milk portunity not only to collect these data but also with high specific heat coming from endother- to facilitate interdisciplinary exchange. mic mothers may serve to warm the young, especially newborns for which ingested milk Other Influences on the Length of Lactation can be a relatively large proportion of neonatal mass. Habitat and Diet. Preliminary analyses of Thus, for some species, the nutritional value the relationships of habitat and diet to the of milk may be of least equal importance to length of lactation (4) suggest that, when they the thermoregulatory, social, or protective are broadly defined, habitat and diet do not functions of lactation. Milk quality and quan- influence the length of lactation across mam- tity may reflect these additional functions of mals (Table 4). However, many taxonomic ord- lactation and not be closely tied to offspring ers of mammals have distinctive habitats (e.g., growth and development.

Journal of Dairy Science Vol. 76, No. 10, 1993 SYMPOSIUM: LIMITS TO LACTATION 3231 Basal Metabolism. The relationship be- dard biological texts give scant attention to this tween basal metabolic rate (BMR) and lacta- central mammalian characteristic, and most tion is complicated (Table 5). Data for age at studies of the phenomenon itself are on the weaning, female mass, and BMR exist for only cellular and molecular aspects. In this com- 180 species, including the three monotremes. parative investigation, temporal and energetic After the effects of mass are removed, BMR is aspects of lactation have been analyzed using negatively correlated with lactation for these species, not cells or molecules, as units. species; i.e., a higher resting metabolism is For mammals, allometric constraints are the related to an earlier age at weaning. However, most important determinants of lactation separate analyses of species with long (44 spe- length. Within smaller phylogenetic subsets of cies) and average (131 species) lactation mammals (orders and families), allometric con- lengths indicate no significant relationships of straints are reduced, or they disappear. Apart BMR with lactation in either group after the from female mass, some reproductive charac- effects of mass are removed. Separate analyses teristics (litter size, neonatal development, and of metatherians (29 species) and eutherians relative nutritional dependency) may operate in (148 species) suggest that BMR has no rela- concert to influence lactation. For instance, tionship to lactation length for marsupials but species with single, precocial young have early is inversely related to the age of weaning in first solid food relative to weaning regardless placental mammals, again, after the effects of of body mass. The age at first solid food may mass are removed. alter the rate or timing of energetic investment Basal metabolic rate is defined for non- during lactation, as do delayed implantation reproductive, nongrowing, feed-deprived, inac- and dispause during gestation. tive . During lactation, neither mothers The coordination and integration of nor offspring fit these criteria. Unfortunately, reproductive characteristics have a profound measures of metabolism in mother and off- impact on the evolution of unitary phenomena, spring pairs during lactation are lacking. Until for example, the lipid content of milk. The such estimates are available for an array of amount of fat in milk may be influenced not mammals, the relationship of metabolism to solely by nutritional needs, but also by the lactation will remain as opaque as milk. selective pressures on a more varied, yet cohe- sive, array of reproductive characteristics. CONCLUSIONS Pleiotropy and polygeny, as well as the social nature of reproduction in general and Lactation defines mammals. As such, un- lactation in particular, weave the molecular derstanding lactation is crucial to understand- and cellular aspects of lactation into the larger ing the biology of mammals. However, stan- fabric of a deme’s reproductive biology. Simi-

TABLE 5. Relationship of lactation length to adult female mass (grams) and basal metabolic rate (BMR) (whole body, milliliters of oxygen per hour) for various mammalian groups.1

2 SlopeMASS SE SlopeBMR SE Constant SE R n F Mammalia .518 .075 -.471 .101 1.528 .077 .40 180 61 Long lactations2 .206* .216 -.006* .276 1.570 .113 .54 44 26 Average lactations3 .210 .062 -.020* .086 1.111 .070 .58 131 90 P = .00l Marsupialia .454* .310 -.354* .399 1.744 .147 .56 29 19 Eutheria .332 .075 -.227 .102 1.339 .079 .40 148 49 P = .027 1 All variables are log10-transformed. Sample size is number of species. Coefficients followed by an asterisk are not significantly different from zero. Unless separately indicated, all other coefficients are statistically significant (P < .0005). 2Includes marsupials (Marsupialia). primates (Primates), and bats (Chiroptera) only. 3Eutherians, excluding primates (Primates), bats (Chiroptera), earless seals (Phocidae), and baleen whales (Mysticeti).

Journal of Dairy Science Vol. 76, No. 10, 1993 3232 HAYSSEN lar patterns (reproductive strategies) may ACKNOWLEDGMENTS emerge, although the particular threads This article is dedicated to the memory of (specific mechanisms) within the design will my brother, Sandy, whose multifaceted ap- vary. proach to both life and death was as compli- Ancestral features of mammalian lactation cated and important to me as the evolution of (and mammalian reproductive biology in lactation is to mammals. general) are the basis for all other future D. Blackbum, B. E. Horner, and S. Tilley modifications. Only primitive aspects will be provided informed and helpful reviews of the the same across a majority of mammals. De- manuscript. rived (selectively advantageous) aspects of lac- tation evolve independently in various line- REFERENCES ages. To ascertain the general applicability of a particular molecular or physiological process, 1 Case, T. J. 1978. On the evolution and adaptive significance of post-natal growth rates in the terrestrial its ancestry must be determined. If the process vertebrates. Q. Rev. Biol. 53:243. is primitive, it may be widespread across mam- 2 Cole, L. C. 1954. The population consequences of life mals; if it is derived, its utility is apt to be history phenomena. Q. Rev. Biol. 29:103. specific to that lineage. Parallel modifications 3 Green, B. 1984. Composition of milk and energetics of growth in marsupials. Symp. Zool. Soc. Lond. 51: may occur independently in other lineages sub- 369. jected to similar selective pressures. However, 4 Hayssen, V. 1985. A comparison of the reproductive the advanced features of lactation in a particu- biology of metatherian (marsupial) and eutherian lar group are germane only for that group, and (placental) mammals with special emphasis on sex differences in the behavior of the opossum, Didelphis not of general applicability. virginiana. Ph.D. Diss., Cornell Univ., Ithaca, NY. The hormonal and metabolic controls of 5 Hayssen, V., and R. C. Lacy. 1985. Basal metabolic lactation in species with widely disparate rates in mammals: taxonomic differences in the allom- etry of BMR and body mass. Comp. Biochem. Phys- suites of reproductive characteristics (for ex- iol. A Comp. Physiol. 81:741. ample, mice and cattle) have evolved under 6 Hayssen, V., R. C. Lacy, and P. J. Parker. 1985. very different selective regimens. On the Metatherian reproduction: transitional or transcending. molecular and cellular levels, only primitive Am. Nat. 126:617. 7 Hayssen, V., A. van Tienhoven, and A. van Tien- features are expected to be similar among hoven. 1993. Asdell’s Patterns of Mammalian mammals with differing reproductive patterns. Reproduction. 3rd ed. Cornell Univ. Press, Ithaca. Physiological or biochemical processes identi- NY. fied as having adaptive value in mice may not 8 Hoaglin, D. C., F. Mosteller, and J. W. Tukey. 1983. Understanding Robust and Exploratory Data Analysis. have similar utility for cows or humans. Broad John Wiley & Sons, New York, NY. physiological similarities in the hormonal con- 9 Snedecor, G. W., and W. G. Cochran. 1980. Statistical trol and metabolism of lactation most likely Methods. 7th ed. Iowa State Univ. Press, Ames. 10 Tyndale-Biscoe, H., and M. Renfree. 1987. Reproduc- represent primitive features of milk production tive Physiology of Marsupials. Cambridge Univ. rather than recent adaptive modifications. Press, Cambridge, Engl. Lactation is the quintessence of mammals. 11 Wilson, D. S. 1980. The Natural Selection of Popula- Mammals are defined by this multifaceted tions and Communities. Benjamin/Cummings Publ., component of their reproduction, which has Menlo Park, CA. influenced their biochemistry, physiology, anatomy, behavior, sociality, ecology, and evo- APPENDIX lution. Understanding how these components Familial common names (or the most popu- are integrated and how they have changed over larly known representative) are listed for orders time offers an unparalleled opportunity for presented in Figures 4 through 7. synthesis across biological disciplines that are Edentata or Xenarthra: Bradypodidae (three- usually disparate. Bridging disciplinary barri- toed sloths), Choloepidae (two-toed sloths), ers, as this symposium does, will eventually Dasypodidae (armadillos), and Myrmecophagi- contribute to a multidimensional understanding dae (anteaters). of lactation as cohesive and intricate as the Insectivora: Chrysochloridae (golden phenomenon itself. moles), Erinaceidae (hedgehogs), Solenodonti-

Journal of Dairy Science Vol. 76, No. 10, 1993 SYMPOSIUM: LIMITS TO LACTATION 3233 dae (solenodons), Soricidae (shrews) Talpidae coenidae (porpoises), Physeteridae (sperm (moles), and Tenrecidae (tenrecs). whales), Platanistidae (river dolphins), and Chiroptera: Emballonuridae (sheath-tailed Ziphiidae (beaked whales). bats), Megadermatidae (false vampire bats), Perissodactyla: Equidae (zebra), Rhinocerot- Molossidae (free-tailed bats), Noctilionidae idae (rhinoceroses), and Tapiridae (tapirs). (bulldog bats), Nycteridae (slit-faced bats), Artiodactyla: Bovidae (antelope), Camelidae Phyllostomidae (leaf-nosed bats), Pteropodidae (camels), Cervidae (deer), Giraffidae (giraffes), (flying foxes), Rhinolophidae (horseshoe bats), Hippopotamidae (hippopotamuses), Suidae Rhinopomatidae (mouse-tailed bats), and (pigs), Tayassuidae (peccaries), and Tragulidae Vespertilionidae (common insectivorous bats). (chevrotains). Primates: Callimiconidae (Goeldi’s mar- Lagomorpha: Leporidae (hares) and moset), Callitrichidae (tamarins), Cebidae Ochotonidae (pikas). (New-world monkeys), Cercopithecidae (Old- Rodentia: Agoutidae (), Aplodontidae world monkeys), Cheirogaleidae (mouse (mountain beavers), Arvicolidae (voles), lemurs), Daubentoniidae (aye-aye), Galigonidae Bathyergidae (African mole rats), Capromyidae (galagos), Hominidae (humans), Indridae (sifa- (hutias), Castoridae (beavers), Caviidae (guinea kas), Lemuridae (lemurs), Lorisidae (lorises), pigs), Chinchillidae (chinchillas), Cricetidae and Pongidae (great apes). (gerbils), Dasyproctidae (agoutis), Dipodidae Carnivora: Canidae (dogs) Felidae (cats), (jerboas), Echmyidae (spiny rats), Erethizonti- Herpestidae (mongooses), Hyaenidae (hyenas), dae (New-world porcupines), Gliridae (dor- Mustelidae (weasels), Odobenidae (walruses), mice), Heteromyidae (kangaroo rats), Hyd- Otariidae (fur seals), Phocidae (earless seals), rochaeridae (capybaras), Hystricidae (Old- Procyonidae (raccoons), Protelidae (aard- world porcupines), Muridae (rats), Myocastori- wolves), Ursidae (bears), and Viverridae (ge- dae (nutrias), Octodontidae (degus), Pedetidae nets). (spring hares), Rhizomyidae (bamboo rats), Cetacea: Balaenopteridae (rorquals), Del- Sciuridae (squirrels), Spalacidae (blind mole phinidae (marine dolphins), Eschrichtidae (grey rats), Thryonomyidae (cane rats), and Zapodi- whales), Monodontidae (white whales), Pho- dae (jumping mice).

Journal of Dairy Science Vol. 76, No. 10, 1993