Humans as inverted bats: A comparative approach to the obstetric conundrum

Abstract

Objectives: The narrow human birth canal evolved in response to multiple opposing selective forces on the pelvis. These factors cannot be sufficiently disentangled in humans because of the limited range of relevant variation. Here, we outline a comparative strategy to study the evolution of human childbirth and to test existing hypotheses in primates and other mammals.

Methods: We combined a literature review with comparative analyses of neonatal and female body and brain mass, using three existing datasets. We also present images of bony pelves of a diverse sample of taxa.

Results: Bats, certain non-human primates, seals, and most ungulates, including whales, have much larger relative neonatal masses than humans, and they all differ in their anatomical adaptations for childbirth. Bats, as a group, are particularly interesting in this context as they give birth to the relatively largest neonates, and their pelvis is highly dimorphic: Whereas males have a fused symphysis, a ligament bridges a large pubic gap in females. The resulting strong demands on the widened and vulnerable pelvic floor likely are relaxed by roosting head-down.

Conclusions: Parturition has constituted a strong selective force in many non-human placentals. We illustrated how the demands on pelvic morphology resulting from locomotion, pelvic floor stability, childbirth, and perhaps also erectile function in males have been traded off differently in mammals, depending on their locomotion and environment. Exploiting the power of a comparative approach, we present new hypotheses and research directions for resolving the obstetric conundrum in humans.

Figure 1

Pelvic orientation, the approximate position of the trunk's center of mass, and the direction of gravity in A, a human; B, a chimpanzee; C, a fruit bat; and D, a sloth, depicted in postures typical for each species. In humans the gravitational force of the visceral organs is exerted directly onto the pelvic floor. In bats and sloths, by contrast, no force is exerted by the visceral organs on the pelvic floor due to the different orientation of the pelvis. (A and B after Whitcome et al., 2017)

Figure 2

Pelves of selected mammal species. Males on the left, females on the right. Collection numbers are given. A, Choloepus hoffmanni (Hoffmann's two‐toed sloth, Xenarthra: Pilosa), NMW 31566 and NMW 3996. B, Macropus rufus (Red kangaroo, Marsupialia: Diprotodontia), NMW 22717 and NMW 22747. C, Nyctalus noctula (Common noctule, Laurasiatheria: Chiroptera), NMW 42194 and NMW 36120. D, Rousettus aegyptiacus (Egyptian fruit bat, Laurasiatheria: Chiroptera), NMW 20840 and NMW 20834. E, Erinaceus roumanicus (Northern white‐breasted hedgehog, Laurasiatheria: Eulipotyphla), NMW 20153 and NMW 968. F, Acinonyx jubatus (Cheetah, Laurasiatheria: Carnivora), NMW 72724 and NMW 70616. G and H, Rangifer tarandus (Reindeer, Laurasiatheria: Cetartiodactyla), male (G) and female (H), NMW 69121 and NMW 68134. For photographs of pelves of additional mammalian taxa, see Supporting Information

Figure 3

Average brain mass versus body mass for 630 mammalian species (data from Boddy et al., 2012a, 2012b). On this log–log scale, the linear regression has a slope of 0.75, reflecting the well‐known negative allometry of brain mass. Cetartiodactyla: even‐toed ungulates, including Cetacea (whales and dolphins), which are nested within the terrestrial artiodactyls. For the number of species by higher‐order taxon, see Table S2 in Supporting Information

Figure 4

A, Relative neonatal body mass (neonatal mass as percentage of maternal mass) versus maternal body mass for 284 mammalian species on a log‐log scale (data from Tague, 2016 and other literature sources, see Supporting Information Table S1). B, Ranking of different mammalian groups according to their relative neonatal body mass. “Fissipedia” refers to the paraphyletic group of terrestrial carnivorans, that is, Carnivora excl. Pinnipedia (seals). Similarly, “Artiodactyla” refers to the paraphyletic terrestrial even‐toed ungulates, that is, Cetartiodactyla excl. Cetacea (whales and dolphins). For the number of species by higher‐order taxon, see Table S2

Figure 5

Relative neonatal brain mass (neonatal brain mass as percentage of maternal body mass) versus female body mass for 109 mammalian species on a log‐log scale (data from Capellini et al., 2010a, 2010b). For an explanation of ‘Artiodactyla’, see caption of Figure 4. For the number of species by higher‐order taxon, see Table S2

Figure 6

Percentage of adult brain mass achieved at birth versus percentage of adult body mass achieved at birth for 59 mammalian species on a log‐log scale (the species covered both by Boddy et al., 2012a, 2012b, and by Capellini et al., 2010a, 2010b). This plot represents an altriciality‐precociality axis separately for the entire body and the brain. For an explanation of ‘Artiodactyla’, see caption of Figure 4. For the number of species by higher‐order taxon, see Table S2