Susan W. Margulis

The ABO blood group is a trans-species polymorphism in primates

The ABO histo-blood group, the critical determinant of transfusion incompatibility, was the first genetic polymorphism discovered in humans. Remarkably, ABO antigens are also polymorphic in many other primates, with the same two amino acid changes responsible for A and B specificity in all species sequenced to date. Whether this recurrence of A and B antigens is the result of an ancient polymorphism maintained across species or due to numerous, more recent instances of convergent evolution has been debated for decades, with a current consensus in support of convergent evolution. We show instead that genetic variation data in humans and gibbons as well as in Old World monkeys are inconsistent with a model of convergent evolution and support the hypothesis of an ancient, multiallelic polymorphism of which some alleles are shared by descent among species. These results demonstrate that the A and B blood groups result from a trans-species polymorphism among distantly related species and has remained under balancing selection for tens of millions of years—to date, the only such example in hominoids and Old World monkeys outside of the major histocompatibility complex.

Relationships among parental inbreeding, parental behaviour and offspring viability in oldfield mice

Studies of inbreeding depression have traditionally suffered from two weaknesses. First, they usually confound offspring deficiencies with parental ones; second, they neglect the possible role of behaviour in inbreeding depression. In the present study, I examined the relationship among parental inbreeding, offspring viability and parental behaviour in two subspecies of the monogamous oldfield mouse, Peromyscus polionotus. Parental inbreeding was separated from any offspring inbreeding effects through both experimental design and analysis. Dams performed more parental behaviour than did sires, and maternal behaviour had a stronger effect on offspring survival than did paternal behaviour. Maternal behaviour was more buffered to the effects of inbreeding than was paternal behaviour; that is, parental behaviour of inbred females was not compromised. In contrast, inbred males showed substantial deficits in parental behaviour, but this did not put their offspring at risk. Although inbred females had lower reproductive success than outbred females, this effect was not manifest in terms of lower offspring viability. Therefore, inbreeding depression manifests itself through deficits on traits of adult females other than maternal care. A possible physiological basis for these findings is hypothesized.Copyright 1998 The Association for the Study of Animal Behaviour.

The effects of inbreeding on testicular sperm concentration in Peromyscus polionotus.

Inbreeding effects on fitness have most often been quantified via juvenile mortality. However, inbred adults may suffer from inbreeding depression if their fertility or fecundity is compromised as a consequence of inbreeding. Here, the effects of inbreeding on male fertility in oldfield mice, Peromyscus polionotus, were examined. Testicular sperm concentration was assessed in 93 males, 68 of which were paired for breeding. Forty of the 68 paired males failed to produce offspring. Total testicular sperm count, sperm count (g testis)(-1), and testis mass all declined significantly with increasing inbreeding coefficient. Sperm concentration did not significantly impact reproductive success. Although sperm concentration in males of most species can decline to low levels before reproductive impairment is detectable, the declines in testicular sperm concentration found here suggest that inbreeding can affect fertility in adult males. Furthermore, monitoring testicular sperm concentration could provide a mechanism to monitor potential declines in reproductive performance before population-level reproductive success is irreparably impaired. The implications for the management of small, captive and wild populations may be substantial.

Behavioral monitoring in zoos and aquariums: a tool for guiding husbandry and directing research.

Behavioral monitoring is the scientific collection of animal behavior data to understand normal patterns of behavior and changes in these patterns. This tool is underutilized in the zoo industry although it can be an effective indicator of many potential problems that compromise zoo animal well-being. We suggest that a behavioral monitoring program should be a core component of a zoological institutions care program. We detail the benefits of such a program and describe its components. We provide guidelines for implementing such a program and make recommendations that will help institutions to employ behavioral monitoring programs with reasonable expense. We argue that the benefits of such a program, primarily increased detection of rising or potential problems, far outweigh the minor costs of implementation.

Sexual and Hormonal Cycles in Geriatric Gorilla gorilla gorilla

As our closest living relatives, great apes likely experience behavioral and physiological patterns associated with reproductive aging and menopause that are similar to human patterns. We present results from a nationwide zoo-based study on behavioral and hormonal changes in female western gorillas. We evaluated progestogen concentrations via daily fecal sampling in 30 gorillas, 22 of which were geriatric (≥30). We collected concurrent behavioral data 1–3 times weekly on 16 of the females. While control females cycled regularly, ca. 23% of geriatric females are acyclic (menopausal), and another 32% show variable hormonal patterns suggesting perimenopause. Patterns included increased variability in cycle length and peak progestogen values, and frequent insufficient increases in progestogen levels during the luteal phase. Acyclic females have significantly lower overall progestogen concentrations than the self cycling females, though differences are not significant when cycle phase is incorporated. We detected behavioral estrus in 9 of 10 cycling females for which data were available. In all but 1 case, proceptive behavior occurred during the follicular phase, preceding ovulation on average by 6.6 d. Females spent more time in proximity to the silverback male while in behavioral estrus than during other periods. To date, maximum longevity in captive female gorillas is 52 yr, with poor reproductive prognosis beginning from the age of 37. We demonstrate that both perimenopause and menopause characterize aged female gorillas, which may experience a postreproductive lifespan of >25% of their lives. Continued study of aging apes is warranted, and apes may serve as models for age-related reproductive changes in humans.

Sex-biased lactational duration in a human population and its reproductive costs.

SummaryWe tested the proposition that among humans (1) differences in lactational duration result in differences in costs of reproduction even under rich nutritional conditions; and (2) elimination of factors postulated to favor male-biased parental care will be reflected in elimination or reversal of sex-biased care. To do so, we examined the relationship between lactational duration and fertility among Hutterites, a communal-living human population in which the levels of nutritional resources and fertility are high, breast-feeding is the norm, contraceptive use is limited and the collective social and economic system results in low resource variance among individuals. We demonstrate that even under good nutritional conditions, duration of nursing was a significant predictor of the length of time to next pregnancy and that nursing continued to suppress fertility after the resumption of menses. Moreover, we find that daughters were nursed longer than sons, leading to a longer interval to next pregnancy. We examine this uncommon, but not unique, finding of female-biased human parental care in the light of Hutterite social structure, and we explore the consistency of this finding with the most applicable models of parental investment.

Differential Effects of Inbreeding at Juvenile and Adult Life-History Stages in Peromyscus polionotus

Inbreeding depression traditionally has been measured at early life-history stages, such as neonatal or juvenile viability or deficits in growth and development. I investigated additional fitness components by evaluating impact of inbreeding on reproductive success of adult females in a captive colony of oldfield mice ( Peromyscus polionotus subgriseus and P. p. rhoadsi ). By first conducting analyses on only inbreeding of litters (i.e., relatedness of parents) and then adding maternal effects (mothers inbreeding coefficient independent of parental relatedness, parity, and maternal inactivity), I illustrated effect of inbreeding on life-history characters that were manifested in adulthood. Young in inbred litters (f > 0.1) tended to be smaller than young in outbred litters, but inbred litters did not exhibit any decrements in survival probability. Number of young raised to weaning from inbred and outbred litters did not differ. Inbred females (inbreeding coefficient f > 0.1) reared significantly fewer young than did outbred females (f < 0.1) (independent of whether parents were related and therefore independent of whether young themselves were inbred). Differences between the two subspecies were found for a number of fitness traits. These differences are attributed to chance differences in genetic makeup of founder stocks (founder effect). Examining inbreeding effects only at a single life-history stage (i.e., during the juvenile period) and only on a single fitness trait (juvenile viability) may result in serious underestimation of the extent of inbreeding depression.

Perimenopause and Menopause: Documenting Life Changes in Aging Female Gorillas

As our closest living relatives, great apes likely experience physiological patterns associated with reproductive aging that are similar to humans. We present results from a nationwide zoo-based study on female western lowland gorillas during which we evaluated concentrations of progestogens via daily fecal sampling in 30 gorillas, 22 of whom were geriatric (>or=30). Whereas control females cycled regularly, ca. 23% of geriatric females were acyclic (menopausal), and approximately 1/3 showed variable hormonal patterns suggestive of perimenopause. Patterns included increased cycle variability, low luteal phase rises of progestogens - possibly indicative of anovulatory cycling - and peak height variability of progestogens in the luteal phase of the cycle. We discovered a progressive trend toward increased variability in estrous cycle length and toward decreased concentrations of fecal progestogens when we compared control to geriatric cycling and to geriatric noncycling females. Noncycling females had significantly lower overall progestogen concentrations than the cycling females, though differences were not significant when cycle phase was incorporated. Preliminary analyses of follow-up data on 10 perimenopausal females indicated that subjects experienced age-related changes in reproductive function that mirrored those observed in aging human females including a female who transitioned from perimenopause to menopause. To date, maximum longevity in captive female gorillas is 52 years, with poor reproductive prognosis beginning from the age of 37 suggesting a postreproductive lifespan of >25%. Continued study of aging apes is warranted, with emphasis on longitudinal monitoring of aged subjects.

Behavioural risk factors in the reproduction of inbred and outbred oldfield mice

The present study investigated two rarely measured aspects of inbreeding depression: the relationship between inbreeding and behaviour, and the possibility that inbred individuals that survive infancy may still suffer from inbreeding depression by failing to breed or failing to show appropriate mating or parental behaviours. Specifically, the relationship between (1) behaviour at pairing and reproductive success, (2) inbreeding and reproductive success and (3) inbreeding and pairing behaviour, was examined in two subspecies of the oldfield mouse, Peromyscus polionotusEffects of parental and offspring inbreeding were separated through experimental design and analysis. Activity level during the first 25 days after pairing predicted future reproductive success: pairs that remained less active during the nocturnal (active) period were significantly less likely to breed than pairs that remained more active. Inbred females took significantly longer to produce their first litters and were less likely to produce litters than were outbred females, independently of whether females were related to their mates (i.e. whether their offspring would be inbred). Inactive pairs averaged fewer surviving pups than did active pairs. Inbreeding coefficient of female was a significant predictor of activity level in one of the two subspecies, suggesting that inbreeding may affect behaviour. Inbred adult females showed inbreeding depression in the form of lower conception rates and fewer surviving offspring, although the specific traits affected differed for the two subspecies. The implications for captive breeding programs, and likely causes of the subspecific differences, are discussed.

Primate Reproductive Aging: From Lemurs to Humans

The scope of data now available for primates from long-term field and captive studies has opened up exciting possibilities for investigating age-related patterns of reproduction. Valuable information on the aging process can be gleaned through broad cross-taxonomic comparative studies that include lemurs, monkeys, apes and humans. Thus, across all taxa discussed in this volume, female reproduction was found to be complex and dynamic, affected by the interplay of multiple exogenous and endogenous factors. Throughout their lives, females differ in their individual reproductive output. As they age, a period of reproductive instability is common among female primates and perimenopausal- like hormonal changes have been noted in many species. Available data from lemurs and callitrichids indicate that at least in some species, age-related declines in reproduction are manifested as diminished success of females to rear their young to weaning age. Few data are available for New World primates, but the same observation holds true for Old World monkey females, who also are characterized by declines in sexual activity and decreased birth rates. In apes, captive data suggest the presence of an appreciable postreproductive lifespan but this has not been confirmed in the wild. Menopause may be manifested as an evolutionary continuum across primate taxa with the potential for an extended postreproductive lifespan evident in cercopithecines and apes.