Wild Moms

I dedicate this book to my amazing, supportive, and wonderful mom, Joanne

. . . and to those silly people who call me mom: Shaeden, Loanna, Faro, and Juna

CONTENTS

Introduction

1

Development Is Diverse

2

The Egg-Content Conundrum

3

Brood Parasitism: An Inconvenient Truth

4

Cooperative Creeds and Communal Cliques

5

Buns in Mammalian Ovens

6

A Pregnant Pause

7

A Child Is Born

8

Newborns and Nightmares

9

Depression and Abuse: Not Just a Human Predicament

10

Mammal Moms and Milk

11

Opportunistic Orphans and Magnanimous Moms

12

Other Mothers: Adoption and Allomothering

13

The Meaning of Weaning

14

Menopausing Moms and Gracious Grandmas

15

Mothers in Mourning

Afterword

References

Acknowledgments

About the Author

Index

INTRODUCTION

It could be argued that motherhood is the most important job that evolution ever made. And yet what it means to be a mom is something that is both impossible to tangibly state and totally obvious to anyone who has done it. We can learn some lessons about our own species by looking at our animal counterparts, and that’s why, as an evolutionary biologist and a mother of four myself (with children who are 12, 10, 8, and 6), I’ve spent a great deal of time studying motherhood in the animal kingdom. The result is Wild Moms. It’s been an extraordinary journey, and the thing that continually surprised me throughout my research has been that, for all the differences between distantly related animals, what is most fascinating is how much we all have in common.

One of the most compelling things I considered as I researched this book is how human mothers vary in our practices as natural animals. After all, our bodies evolved to survive and reproduce, and the former certainly doesn’t mean much without the latter. In my own way, I somehow just knew when I was ready for motherhood. It happened fairly fast—and interestingly, prior to that point, I really wasn’t sure when or if I would even have children. It’s almost like a switch went off inside my body and brain, and suddenly I could not get pregnant fast enough. I was obsessed with babies, getting pregnant, and learning what I could do to facilitate that process. The strange way in which my body decided I was ready for motherhood always left me wondering whether any other animal moms out there feel the same way. Although as observational scientists we aren’t yet in a position to simply ask animals about their feelings and emotions about various aspects of their lives, recent research on the emotional and cognitive capabilities of animals allows us to conclude that there is most definitely a level of awareness and sensitivity in many members of the animal kingdom. Animals form relationships, they empathize, they love. What could possibly be more significant for any female (mammal, fish, or bird) than to undertake the process of motherhood?

Now that my kids are a little older, I’m able to reflect more on my experience and what it means in the context in the rest of the animal kingdom. Let’s face it: for those first few years, any human mother is running off her feet just trying to ensure that her infants survive. There are countless feedings, changes, fussiness, and tremendous exhaustion. It’s so difficult, and yet supposedly so natural. Well, it turns out that while much of our experience matches that of our animal counterparts, human mothers are guilty of complicating the process to extents that are unprecedented in the animal kingdom. We will learn in this book that while modern technologies and Western lifestyles allow for an increased level of comfort and support, there is simply no level of wealth or materialism that can replace what the body is naturally meant to do. Women can be amazing mothers without all the bells and whistles that many modern practices require. Just because chimpanzee mothers do it without bottles, strollers, formula, or diapers doesn’t mean that they are any less maternal than human mothers. In fact, there are many cases in which I would consider our lavish developments to make our mothering practices less natural than those of the rest of the animal kingdom—although that’s a topic for another book.

Wild Moms sees the reader through the process of motherhood, from the unfertilized egg to becoming a grandmother. In all chapters, I highlight examples of the ways that animal moms address the same kinds of issues that human moms have. This book is of course far from exhaustive; a complete volume of motherhood could (and should) be many times longer than this. However, you can rest assured that I’ve included a wealth of information that is interesting, educational, and poignant.

Overall, I hope that this book opens your eyes to the diverse and amazing world of motherhood on our planet. I’ve spent so much time on this topic, yet sometimes I feel as though I have barely scratched the surface. My hope is that Wild Moms will be an exciting introduction to the simultaneous diversity and sameness of motherhood. My overall conclusion is one that I’ve always carried with me when it comes to raising my own children: That there isn’t just one way to be successful. If we define success as the survival of an infant to sexual maturity, then there are as many ways to be successful as there are moms out there doing it. In most animals, including primates, this is where our measurement of motherhood largely stops. In our own species, however, it seems that we have taken this issue and made it into a new kind of problem—that of infants who remain dependent long after sexual maturity takes place. I suppose that’s a topic for another book, but suffice it to say, that human moms have a lot more in common with the rest of the primate order than we sometimes like to think.

Thank you for your interest, and happy reading!

1

DEVELOPMENT IS DIVERSE

Human moms, like most other mammals, gestate their babies during a phase of pregnancy. Simply put, we cook the buns in our ovens and spit them out when they are done. This is called viviparity, the biological term used to describe the act of one animal gestating a live offspring inside its own body. Vivi translates to alive and parity translates to reproduction, so pregnancy and live birth aptly translates to ‘living reproduction. This is obviously just one way for any female to become a mom, but there are of course many other paths to motherhood that don’t involve pregnancy or live birth. There is a vast diversity of different strategies out there for how females in the animal kingdom become moms.

Many aquatic invertebrate animals sexually reproduce by means of something called broadcast spawning. Most of these animals are either sessile (meaning that they are fixed to the ground in either a burrow, shell, integument, or some other kind of casing that prevents them from moving around, like tunicates or corals) or else they move very slowly (as with seastars or anemones). Since adult movement is not a major factor for these creatures and since they live in an aquatic environment which serves as a convenient medium through which to share their sexual prospects, broadcast spawning represents an evolutionarily stable and successful strategy for sexual reproduction. Billions of gametes (defined as the combination of sperm and egg) are spewed into the surrounding environment of the ocean, and happy invertebrate mothers breathe sighs of relief that their parental duties are thus complete.

Although it sounds quite simple to be a broadcast spawner, the fact of the matter is that successful broadcasters are attentive to a wide range of environmental characteristics. Spewing one’s genetic blueprints into the world without a care for whether they meet a suitable counterpart would be an unwise thing for any mom to do—seastar, snail, crab, or otherwise. It’s true that maternal duties are minimal in broadcast spawners, but the timing of gamete release is among the most important aspects for any individual’s reproductive success. The most fruitful strategies take into consideration both the availability of potential mates (specifically mates who are also ready to reproduce sexually) and environmental characteristics like currents, tides, predator density, and water temperature. Individuals of several species take cues from lunar cycles, which are predictable and repeatable processes easily observable from many vantage points, as there is ample reason to broadcast simultaneously with those around you. In fact, during phases of invertebrate spawning, it’s common for the surrounding water to become cloudy with the sexual products of several individuals of several species, a veritable soup of sperm and eggs all madly trying to reach the correct partners at the correct time.

Another factor that broadcasters must take into account is density of potential partners and potential competitors. Conditions can change at a moment’s notice, and triumphant individuals will be those who are able to process information in a timely manner. Too many or not enough spawners could spell disaster for an individual’s reproductive success. Eggs that do not come into contact with the appropriate sperm will go unfertilized; however, eggs that come into contact with too much sperm could be susceptible to polyspermy (multiple fertilization), which renders them useless. Although broadcasting sounds like an effective way to get the job done, it could be detrimental for individual reproductive success if gamete densities become too high.

Many broadcast spawning mothers are also fathers. Hermaphrodites are common in the invertebrate world, and a large proportion of aquatic invertebrates have both male and female reproductive organs. That’s not to say that these individuals can simply fertilize their own gametes and not participate in sex with others. There are species where this is possible, but it’s generally better for genetic diversity to cross-mate with either one or more outside individuals, in the same way that humans avoid incest to avoid the potential negative effects of recessive alleles (genetic abnormalities that are normally masked through outbreeding). In a pinch, one may fertilize oneself if the environment isn’t conducive to successful fertilization with an outside partner, but it’s always better in terms of biological fitness to diversify the genetic lineage so as to hedge your bets that at least some of the offspring will survive.

Genetic diversity is indeed an important aspect of reproduction for all mothers, but in several species females can produce genetic clones of themselves asexually, in a process called parthenogenesis or thelytoky. While this process does not require a genetic contribution from a male (sperm), most parthenogenetic females can also reproduce sexually when the opportunity presents itself. In fact, a female may choose a complex course of reproductive options depending on the environmental cues that she experiences at a given time. When would a female choose to simply clone herself over accepting a genetic donation from a male partner? In some cases, males may not be available, or it may be wise for a female to reproduce in the fastest way possible due to external factors like predation risk. Being able to clone one’s self is a pretty interesting way to be able to maximize one’s biological fitness in the face of environmental stochasticity (unpredictability), sexually transmitted diseases, or immediate predation risk.

In addition to having the ability to clone themselves through asexual reproduction, the female springbok mantis (a terrestrial invertebrate closely related to other more recognizable praying mantis species) also engages in cannibalism of their potential male partners. In this species females cannibalize males before any sexual activity. In other words, males are often nothing more than a light snack for hungry females who reserve the ability to clone themselves instead of mating with them. It’s a bit of a double whammy for males of this species—not only is their sperm on a take-it-or-leave-it basis with potential female partners, but they also stand to lose their lives even before they get a chance to share it.

It turns out to be the age of females that is the most likely predictor of their behavior toward males. These ladies become less aggressive and more likely to mate sexually as they age. This is a common theme in many sexually cannibalistic females. Initially, they get their bodies in prime mothering condition by ingesting a few sexually mature males. Reproducing asexually through pathogenesis allows these females to cannibalize males at a high frequency while they still maintain the ability to pass on their genetic blueprints. However, later in life when their bodies are in prime condition for reproducing sexually, females switch reproductive modes. This scenario is described by the adaptive foraging hypothesis, which predicts a decrease in cannibalism as females age and an increase in fecundity of the females who engage in it.

Females who can reproduce asexually aren’t always the ones in the driver’s seat. There are certain bacterial or viral endosymbionts (organisms that live and reproduce exclusively within another) that can force clonal reproduction in their hosts. This is common in arthropods (which are segmented invertebrates including insects and arachnids). The endosymbionts work to increase their own biological fitness by inducing asexual reproduction in their female hosts. Can you imagine if your own body just reproduced without any kind of decision to do so on your part? This is the unfortunate reality for over 124 species in seven various arthropod categories. The bacterial genus Wolbachia is the culprit, causing unsuspecting females across the world to become asexual mothers without their knowledge or consent. Females in question aren’t harmed by this lack of control over their (asexual) reproductive lives; they maintain the ability to reproduce sexually when an appropriate opportunity presents itself.

Broadcast spawning and parthenogenesis are two ways that female animals become moms, but they aren’t the routes that are normally associated with the process. As mentioned above, viviparity loosely translates to alive reproduction, while oviparity refers to egg reproduction. Whether offspring are produced through viviparity or oviparity, a male cannot be sure of his paternity; but in species in which eggs are laid early in development and require tending, protection, or incubation, he may make a substantial paternal investment. This is because dads can do something to help since the embryos are outside of the mother’s body. (That of course is not the case in most mammalian species where the egg is internally fertilized.)

There is an extensive array of ways in which oviparity takes place in the animal kingdom. In some species, mothers construct elaborate nests, burrows, or hiding spots for egg incubation; in other species, embryos are attached to the mother’s body in a specialized pouch or in a crevasse on her body, or they are otherwise carefully guarded until they hatch. The type and extent of egg care is largely dictated by the ecology of the species in question and by the order in which egg extrusion and fertilization occur. If fertilization comes before egg-laying, females lay embryos rather than eggs. Many invertebrate, fish, and amphibian mothers lay egg cases filled with fertilized embryos after they copulate with males and receive sperm. However, if fertilization occurs after the fact, females lay eggs (not embryos) that then receive sperm from nearby males. The number of eggs or embryos depends on the mother’s strategy for pre-hatching care. If she knows she won’t be around, she may lay hundreds or thousands of eggs to increase the chance that some of them will develop into adulthood. If she or the father is going to be able to stick around and care for the potential offspring, there will usually be fewer.

One important aspect of egg-case biology is that not all offspring are created equally. Mothers provide some embryos within the egg case with nutritional advantages; neglected embryos become nothing more than a snack for their own brothers or sisters. It’s Game of Thrones: Egg Case Edition, in which some embryos are destined for survival and others destined to die horrific deaths at the hands of their siblings. For example, a few species of marine snails engage in something called accidental cannibalism. Occasionally, early developing embryos ingest younger embryos, which continue to develop once they are in the first embryo’s gut. The ingested embryo eventually bursts free from its cannibalistic sibling, killing it in the process. It can then engage in something called oophagy, or the ingestion of its sibling’s leftover parts.

Terrestrial invertebrates also lay egg clutches. These aren’t necessarily encapsulated together but instead are laid close together in the same area. For example, female flies of various species lay egg clutches in microhabitats according to environmental cues like resource availability or competition from other females. Eggs can be concentrated onto specific resource patches—like a pile of dung, a tree hole, a specific plant, or a dead carcass—that seem like they might present some developmental advantages. These moms fine-tune both the number and sex of the embryos that they deposit to maximize the eggs’ own individual probabilities for reproductive success.

The most straightforward strategy is simply overproducing offspring without providing specific advantages to any of them. Mothers then let their offspring duke it out for survival within their own egg-case groups. In this way, the strongest, fittest offspring survive and have an excellent chance of making it to sexual maturity themselves. Indeed, females often lay more than ten times the number of eggs that survive to adulthood. These embryos—who had been forced to fight for their lives before they had a chance to be born—are a far cry from the completely helpless newborns of our own species.

It may seem somewhat heartless for a mom of any kind to create more than enough offspring, but there are several well-founded hypotheses for why this may occur. The first reason is explained by the siblicide advantage hypothesis, in which the strongest and largest (often the first hatched) embryos cannibalize their own siblings and realize the twofold benefit of less overall competition and increased body mass and nutrition. The predator satiation hypothesis suggests that moms who lay more than enough offspring stand a better chance at having at least a few of them survive a predator attack. Lastly, the insurance policy hypothesis suggests that mothers may create more offspring so that they can be biologically covered in the event of an environmental disturbance or hatching failure. It’s important to keep in mind that most species exhibit some kind of flexibility in terms of the specific number of embryos or strategy that can be used in a given situation. Unlike most mammals, many invertebrates display a remarkable level of reproductive variability.

As I mention above, in many species, females and males engage in copulation prior to the laying of already-fertilized eggs, whereas in other species, females lay eggs that are externally fertilized by males after the fact. This is a key point in the ecology of many fish species exhibiting the latter, as females may simply take off and leave their eggs to a male to fertilize and then care for. For example, in some bony fish species like salmon and trout, mothers will dig out small nests or redds in benthic (bottom) areas of various marine and freshwater environments. They use their tails to excavate depressions in the substrate, into which they then deposit their eggs. Some females will remain with their eggs once they are fertilized; however, most will leave all egg guarding and maintenance to the father. Since males are often defending a territory, females can choose where to lay their eggs based on qualities of the territory, or on characteristics of the male himself. In many species females are more likely to deposit their eggs into the nest of a male that already has some—since this indicates that other females have chosen him, he’s likely a good provider.

In fish species that are externally fertilizing, males ordinarily take over the bulk of embryonic care once females have left their eggs behind. However, there are always exceptions to any generalization in the animal kingdom. For example, female mouth-brooding cichlids in Lake Tanganyika do not leave their eggs to the care of a specific male. Instead, once they have extruded their eggs, they scoop them back up into their own mouths. Females then solicit sperm donations from various potential fathers. Since it’s best for a female to maximize the genetic diversity of her offspring, she may seek the sperm of several males for fertilization. Females keep the fertilized embryos in their mouths for the duration of their gestation, and new hatchlings will continue to seek protection in mom’s mouth for a short time after they hatch. Although it’s a strange sight to imagine (a female accepting sperm into her mouth from several males in sequence), a mom’s gotta do what a mom’s gotta do!

External fertilization and egg-guarding by males is more often the rule in fish. Although egg laying takes place in some of these species too, in the cartilaginous fishes (such as sharks and rays) copulation, internal gestation, and viviparity are more common, and it’s in these species that we expect to see the greatest level of maternal care. Chondrichthyans (cartilaginous fishes) have a diverse set of reproductive modes, with strategies that range from egg laying to bearing of live young to physiologically complex placental development and nutrition of developing embryos. Shark reproduction is notoriously difficult to study, and sexual reproduction varies substantially between genera. For example, female sand tiger sharks exhibit a remarkable reproductive mode that combines elements of both oviparity and viviparity; this hybrid form of reproduction is called ovoviviparity.

Females give birth to live young that have been nourished by egg yolks inside the uterine cavity. There is no nutritive connection between mother and babies once the fertilized eggs are laid within her own body, which is quite different from the direct nutritive connections (e.g. placenta) that occur in purely viviparous species. Female sand tiger sharks have a pair of uteri, and embryos travel to one of the females’ uteri where they remain for a further period of gestation after being fertilized. However, the first embryo in each uterus to reach 2.1 to 2.3 inches in length hatches and then begins a period of exponential growth as it systematically attacks, kills, and cannibalizes all its siblings in that uterine environment. Once the siblings have all been ingested and the hatchling has reached a size of approximately 4 inches in length, it will begin to feast on the unfertilized ova that have accumulated in the mother’s uterus. Imagine all this action taking place within one’s body while one simply carries on with the day-to-day tasks of life. A veritable war is taking place within her uteri, and female sharks need only wait for the fittest and strongest offspring to emerge at birth. They will be approximately 37½ to 50 inches at this point and will have few predators for the rest of their lives. What this means for sand tiger shark moms is that the strongest, fittest juveniles will triumph from a war that takes place before her babies are even independent. Moms can seek sperm donations from a variety of potential fathers, but only the sperm of the very fittest males will be the successful sire of her offspring. In this way, a female can be behaviorally polygynous but functionally monogamous from each uterus.

Egg-laying is thought to be the ancestral form of creating offspring through sexual reproduction, and most vertebrates continue to utilize it in a number of diverse ways. However, the bearing of live offspring has evolved more than 150 times in the vertebrate groups (apart from birds and jawless fishes), making it one of the greatest examples of convergent evolution. Viviparity has evolved independently in mammals, reptiles, amphibians, and fish. By contrast, lactation evolved once; endothermy and powered flight evolved three times. What does this mean exactly? It means that there are many benefits of internal gestation and live birthing. Such biological benefits have allowed for its repeated, independent evolution in several animal groups. Live birth is advantageous because it can provide enhanced offspring survival, the ability to exploit novel ecological niches, and an increase in the energetic efficiency of the entire reproductive process.

Viviparous vertebrates provide energy to developing offspring in a variety of ways. Matrotrophy, for example, is the provision of nutrition from a mother via a placenta or other means such as through secretory tissues or glands that allow for fetal absorption or ingestion of nutrients. In addition to nutrition derived from direct matrotrophy, there is also something called lecithotrophy, in which nutrition comes from within the egg. This can happen in both egg-laying and live-bearing animals; egg-laying animals are exclusively lecithotrophic, whereas viviparous animals can be both lecitotrophic and matrotrophic if embryos receive at least some of their nutrition from an egg yolk during their internal gestation.

Matrotrophy can be further divided into six categories. There is oophagy (in which sibling yolks or products of siblings are used as nutrition), embryophagy or adelphophagy (in which cannibalism of siblings occurs), histophagy (in which nutrients are ingested in liquid form), macrophagy (in which the mother’s own tissues are used as offspring nutrition), histotrophy (in which nutrients travel from mom to offspring via diffusion), and placentotrophy, (in which nutrients are supplied to offspring through a placenta).