Because humans are mammals with sexual reproduction, people are familiar with the concept of pregnancy, that is with the otherwise outlandish notion that one individual carries a genetically different individual inside its body for an extended period of time before expelling the latter through an orifice. If you are a man, you might feel relieved that this weighty reproductive imposition has been delegated to females in Homo sapiens; and if you are a woman, the thought of becoming pregnant might elicit any of a gamut of emotions ranging from joy to fear or loathing, depending on the circumstances.
One day when I was about 8 years old, I had an insight: God had arranged things equitably for men and women. A man could anticipate being drafted into 2 years of military combat whereas a woman might spend on average about 2 years of life in a state of pregnancy (which I imagined to be an equally unpleasant sentence). This childhood revelation is silly, but in some ways it was prescient. For my generation, about 60 000 young American men died and 160 000 were wounded in Vietnam; whereas across those same years (1959–1975) nearly 10 000 young women lost their lives in the United States and tens of thousands suffered enduring medical disabilities from complications of pregnancy (Kaunitz et al., 1985). Furthermore, on a global scale in recent decades, armed combat has claimed the lives more than half a million young men annually (GBAV, 2008); but ‘maternal mortality’ (defined as a mother's death related to pregnancy) likewise has exceeded 500 000 women per year (Hill et al., 2007). These morbid statistics suggest that my childhood musings about the tribulations of the sexes contained a kernel of truth: young men and women have heavy but different crosses to bear. The statistics also remind us that that pregnancy is a focal time of death as well as birth.
Although nearly all mammals gestate embryos inside the dam's body, female pregnancy is far from universal in the biological world and there are even some species in which males alone become pregnant. Alternative gestational modes permit comparative analyses of how different expressions of pregnancy might impact the evolutionary ground rules for selection pressures on males versus females. With respect to sexual selection, pregnancy entails an asymmetric energetic investment in offspring by the two parents and thereby should have major consequences for the evolution of reproductive behaviors and mating systems. With respect to natural selection, pregnancy occupies a key intersection between the two major components of personal genetic fitness: survival and reproduction. Especially when a placenta physically connects parent with child, pregnancy also provides a uniquely intimate nexus between successive generations. Both of these biological junctures (between parent and child and between survival and reproduction) generate evolutionary conflicts of interest between a mother and her offspring that can be just as consequential for procreation as are conflicts between males over scarce resources and mates.
Webster's dictionary defines pregnancy as ‘having a child or other offspring developing in the body’ whereas my Chambers dictionary describes the condition simply as being ‘with child or young’. Both definitions can be relevant depending on the context. I will apply Webster's definition to animals such as mammals and some fish species in which a pregnant individual (usually a female but sometimes a male) carries embryos inside its body before giving birth to live young. This is viviparous ‘internal pregnancy’, regardless of the extent to which a parent offers resources other than brood space to its young. I will also take advantage of the ambiguity in Chambers′ definition by extending the meaning of pregnancy to encompass situations in which a parent carries offspring on its body in what in effect becomes an ‘external pregnancy’. I will even extend the notion of pregnancy to include oviparous nest-tending fishes in which the embryos that a parent supports are physically separate from the caretaker's body.
With respect to empirical studies of mating systems and sexual selection in the context of pregnancy, genetic parentage analyses based on highly polymorphic microsatellite markers have been popular. For any type of pregnancy, successful mating events (those that yield progeny) by the adult caregiver are relatively straightforward to deduce via molecular parentage analyses because embryos in each brood are physically associated with their pregnant sire or dam. For example, paternity in female-pregnant species can be determined by subtracting known maternal alleles from each offspring's diploid genotype, and thereby deducing which males had mated successfully with the dam of each assayed brood. By contrast, documenting mating behaviors by members of the non-pregnant sex is much more problematic because each such individual may have parented additional broods that were not included in the genetic assays (Jones & Ardren, 2003). Thus, the logistics of parentage analysis make molecular markers ideally suited for quantifying multiple paternity (polyandry by females) within the broods of female-pregnant species and multiple maternity (polygyny by males) within the broods of male-pregnant species, rather than the converse (Avise et al., 2002; Avise & Liu, 2010, 2011).
With respect to the conceptual foundations of selection in the context of pregnancy, ‘parental investment’ theory (Trivers, 1972; Parker & Simmons, 1996) has been especially important as an adjunct to standard mating-system theories (e.g. Bateman, 1948; Orians, 1969; Emlen & Oring, 1977; Arnold & Duvall, 1994). One standard evolutionary train of thought is as follows: beginning early in the evolutionary history of multicellular sexual life, anisogamy promoted gametic retention by females and gametic dispersion by males, and these gender-specific proclivities in turn often promoted within-female syngamy (internal fertilization), which in turn predisposed the female sex to evolve pregnancy-like phenomena, which in turn makes females even more of a limiting reproductive resource compared with males, which further amplifies the evolutionary authority of females over reproductive affairs, which in turn further impacts the operation of sexual selection and thereby amplifies the proverbial ‘battle between the sexes.’
Seven broader evolutionary revelations
(1) Pregnancy entails conflicts as well as cooperation
Pregnancy might seem to be the ultimate collaborative endeavor between individuals because (1) a mother and her fetus both have a vested personal interest in a successful outcome; and (2) so too does the father. Indeed, all three participants (sire, dam and fetus) would seem to share a mutual concern that progeny are born healthy after a productive incubation. On the other hand, each female mammal alone bears the physical burden of incubation and nursing whereas the sire may have little or no reproductive involvement beyond his original genetic contribution. Furthermore, in most sexual species, each family member has a unique genotype, implying that a gene's optimal tactic for self-perpetuation might depend to some degree on which individuals house that gene and any of its copies. Also, the selfish genetic interests of interacting organisms tend to be aligned only insofar as those individuals are related (Hamilton, 1964; Mock & Parker, 1997), and pairs of individuals in a nuclear family differ dramatically in their coefficients of genetic relatedness (r): a mother and her offspring normally share half their genes (r = 0.5) as do full sibs in a multi-birth litter; but half-sib progeny share only one-quarter of their genes (r = 0.25), and a sire and dam typically are unrelated (r = 0.0).
For these and other reasons, each nuclear family is not simply a serene setting for harmonious interactions, but rather it can be an evolutionary minefield of oft-competing genetic fitness interests, both inter- and intragenerational (Trivers, 1972, 1974; Hausfater & Hrdy, 1984; Parmigiani and Vom Saal, 1994; Hudson & Trillmich, 2008). Furthermore, many of these conflicts play out forcefully within the mammalian womb. Thus, pregnancy becomes an evolutionary theatre for intergenerational conflict over parental resources – each offspring is under selection to seek as many maternal resources as possible (limited only by any negative effects on its inclusive fitness that such demands impose on copies of its genes carried by its kin), whereas a dam can be expected to resist excessive demands by the fetus. The net result of each such evolutionary ‘tug-of-war’ (Moore & Haig, 1991) between mother and child is some ontogenetic balance in which each offspring must settle for fewer maternal resources than it ideally might wish and a mother surrenders more resources than she otherwise might prefer. But by evolutionary reckoning, any such maternal–fetal compromise during or after a pregnancy is less the result of a harmonious mutualism than it is an outcome of conflict mediation (Haig, 1993, 1999, 2010; Nesse & Williams, 1994). Of course, maternal–offspring relations entail elements of cooperation as well as conflict; these two categories of interaction need not always be interpreted as mutually exclusive (Strassmann et al., 2011).
(2) Genomic imprinting is a remarkable ramification of pregnancy
Selective pressures that pregnancy promotes sometimes have led to outcomes that catch researchers totally off-guard. One such phenomenon is genetic imprinting: a situation in which a gene is expressed in progeny when inherited from one parent but not from the other (Solter, 1988). In such cases, a gene can have very different effects on offspring (and therefore on the course of a pregnancy) depending on whether it was transmitted via the dam (egg) or sire (sperm). Genetic imprinting in animals appears to be confined mostly to viviparous mammals, but the phenomenon also is common in plants (Feil & Berger, 2007). In recent years, scientists have discovered imprinted genes in many marsupial and placental mammals, including Homo sapiens, where imprinting has been documented at approximately 100 loci to date. Mechanistically, imprinting usually results from the addition of methyl (–CH3) groups to particular nucleotides during the production of male or female gametes, resulting in the specific inactivation of either maternal or paternal genes in offspring (Reik & Walter, 2001). The terms padumnal and madumnal refer to paternally and maternally derived alleles in offspring, so genetic imprinting essentially involves altered expressions of madumnal or padumnal alleles (Haig, 1996).
Haig (1993) introduced evolutionary interpretations for genetic imprinting (and for various other expressions of conflict during mammalian pregnancy) when he wrote:
The effects of natural selection on genes expressed in fetuses may be opposed by the effects of natural selection on genes expressed in mothers. In this sense, a genetic conflict can be said to exist between maternal and fetal genes. Fetal genes will be selected to increase the transfer of nutrients to their fetus, and maternal genes will be selected to limit transfers in excess of some maternal optimum. Thus a process of evolutionary escalation is predicted in which fetal actions are opposed by maternal countermeasures. The phenomenon of genomic imprinting means that a similar conflict exists within fetal cells between genes that are expressed when maternally derived, and genes that are expressed when paternally derived.
Haig's seminal idea has become known as the conflict hypothesis or the kinship hypothesis for genetic imprinting and it still remains the leading evolutionary explanation for the imprinting phenomenon.
Unfortunately, these strategic battles between madumnal and padumnal genes in utero come not without serious medical consequences, especially for embryos that are caught in the evolutionary crossfires (e.g. Haig, 2004). For example, Frank & Crespi (2011) suggest that such intragenomic conflict may affect the regulation of embryonic growth in ways that can precipitate various pathologies such as some cancers as well as psychiatric disorders including some cases of autism and schizophrenia. These authors view evolutionary-genetic conflict as sexual antagonism that can lead to pathologies whenever opposing genetic interests that normally are precariously balanced become unbalanced for any reason. Burt & Trivers (2006) have extended this kind of evolutionary argumentation about intergenic strife to a broad spectrum of otherwise puzzling empirical properties of sexual genomes.
(3) Not all aspects of pregnancy have been shaped by natural selection
Even among mammals, various expressions of pregnancy sometime have and sometimes have not been forged by natural selection. For example, embryonic diapause wherein a delay occurs between fertilization and implantation is a polyphyletic condition that clearly demands an adaptive explanation (related in this case to differences in optimal times for mating vs. birthing); whereas sporadic polyembryony (the occasional production of monozygotic twins) is an idiosyncratic happening that almost certainly is not adaptive per se. And other expressions of pregnancy (such as constitutive dizygotic twinning in marmosets and tamarins; Signer, Anzenberger & Jeffreys, 2000) have some biological elements that do and other elements that probably do not require adaptive explication.
(4) Pregnancy is not always a black-or-white condition
Viviparity (‘live-bearing’) is often viewed as the antithesis of oviparity (egg-laying), but in fact these two reproductive modes are just signposts along a continuum of gestational systems. Many fish and other vertebrate species are ovoviviparous, meaning that gravid females carry internally fertilized eggs that hatch within a dam before she gives birth to live young. Furthermore, a remarkable diversity of gestational phenomena in the biological world gives added testimony to the sentiment that pregnancy is not invariably the all-or-nothing syndrome that we mammals otherwise might assume. For example, pregnancies in various animal species can show gradations in many features including the site of fertilization, the exact location and duration of embryonic incubation within or near the parent, the size of a brood, the mechanism and magnitude of material exchange between the pregnant adult and embryos, and even the sex of the gestating parent. The wide variety of ways and means by which parents nurture early lifestages of their progeny adds spice to scientific studies of pregnancy and related incubational phenomena.
(5) Internal male-pregnancy affords mirror-image vantages on sexual selection and mating systems
Males (rather than females) become pregnant in all of the more than 200 extant species of pipefishes and seahorses (Syngnathidae). The process begins when a gravid female transfers some or all of her many ova to the male's abdomen or tail, where the eggs either are glued onto his external surface or deposited in a specialized pouch that evolved expressly for this purpose. In species with pouches, the male then fertilizes the clutch internally, seals the pouch, and carries the embryos for several weeks before giving birth to live young. During this pregnancy, the sire nourishes, aerates, osmoregulates and protects his brood whereas the mother provides no care for her offspring. To evaluate the evolutionary history and selective consequences of male-pregnancy in syngnathids, researchers have employed PCM (Avise, 2006), with the results often interpreted in conjunction with findings from extensive molecular parentage analyses of genetic mating systems (Jones & Avise, 2001).
The PCM analyses uncovered a good agreement between clade membership and brood-pouch morphology and generally were consistent with the hypothesis that brood pouches with simple designs evolutionarily predated pouches with more complex architectures (Wilson et al., 2003). Results from the genetic parentage analyses of broods confirmed (as expected) that pregnant males invariably have sired the embryos that they carry. Furthermore, these findings coupled with genetic appraisals of maternity helped to confirm the following: (1) many (but not all) syngnathids are ‘sex-role-reversed’ (Vincent et al., 1992; Jones et al., 2005) in the sense that sexual selection operates more strongly on females than on males (Jones et al., 2000); (2) the direction and intensity of sexual selection generally match expectations based on genetic mating systems that proved to range from monogamy to polygynandry to polyandry in various syngnathid species (Jones & Avise, 2001); and (3) all of these outcomes regarding mating behaviors, sexual dimorphism and sexual selection in the male-pregnant fishes differ diametrically from those that typify female-pregnant fishes and many other vertebrate taxa with more ‘conventional’ sex roles.
(6) External male-pregnancy offers even more vantages on sexual selection and mating systems
Approximately 89 of 422 taxonomic families of bony fish (21%) contain at least some species with parental care of offspring, and in nearly 70% of such cases the primary or exclusive parental custodian is the male (Blumer, 1979, 1982). Apart from the syngnathid fishes with internal male-pregnancy, parental care in fish species entails phenomena such as nesting, oral brooding and egg-toting, all of which in effect can be thought of as modes of ‘external pregnancy’ because they too imply a substantial energetic investment in offspring by members of the brooding sex.
Exclusive paternal care of offspring is otherwise quite uncommon in the biological world, so fish again offer mirror-image evolutionary perspectives on parental investment compared with many other animal groups in which females typically are the primary caregivers (Clutton-Brock, 1991). However, an added complication for species with external (as opposed to internal) male-pregnancy is that a bourgeois or nest-tending male sometimes might be cuckolded via ‘extra-pair’ fertilization events (DeWoody & Avise, 2001). Genetic markers as applied to embryos in the nests of many nest-tending fish species have confirmed that foster parentage is indeed common and can arise via several routes including ‘stolen fertilizations’ by sneaker or satellite males (DeWoody et al., 1998, 2000; Neff, 2001) as well as by egg thievery (Jones, Östlund-Nilsson & Avise, 1998) and/or nest piracy. Genetic parentage analyses in nest-tending fish species similarly have been used to address many additional reproductive phenomena including egg mimicry and female choice of mates (Porter, Fiumera & Avise, 2002), filial cannibalism (DeWoody et al., 2001), and alternative reproductive tactics by females as well as by males (Taborsky, 1994; Gross, 1996; Henson & Warner, 1997).
(7) Rates of polygamy are logistically constrained
Evolutionary biologists ever since Bateman (1948) have appreciated that members of the non-pregnant or non-gravid sex (usually males) tend to evolve behavioral dispositions to seek copulations with members of the pregnant or gravid gender (usually females). Thus, when molecular markers were introduced to mating-system analyses in the 1970s, many researchers were intrigued by what they interpreted to be unexpectedly high rates of polygamy in many species suspected from field observations to be mostly monogamous (reviews in Burke, 1989; Avise, 1994; Griffith, Owens & Thuman, 2002). In particular, a research tradition arose wherein a primary goal was to explain why multiple mating by females (polyandry) was far more common that previously thought. For example, as Birkhead (2010) noted in his inaugural THH review, ‘The major unanswered question in post-copulatory sexual selection is the adaptive significance of female promiscuity’. Many hypotheses were advanced and tested in numerous taxa regarding possible direct and indirect fitness benefits that females might derive from polyandry (e.g. Keller & Reeve, 1995; Yasui, 1998; Jennions & Petrie, 2000; Möller & Jennions, 2001). Of course, multiple mating was recognized to have potential downsides as well (such as the risk of contracting sexually transmitted diseases), but overall the bulk of the research effort went into understanding why females (in addition to males) often take multiple mates.
Recent surveys of the literature on genetic parentage in ‘pregnant’ vertebrate and invertebrate animals (Avise & Liu, 2010, 2011; Avise, Tatarenkov & Liu, 2011) have confirmed that the majority of broods do indeed consist of multiple full-sib cohorts, meaning that a gestating parent typically had several successful mates. Much more surprising, however, were two additional genetic observations: (1) the overall numbers and frequency distributions of mates per brood proved to be remarkably similar across invertebrate and vertebrate taxa; and (2) numbers of mates per pregnancy (typically about 2–5) were much lower than they theoretically could have been given the resolving powers of the molecular markers employed and given the large brood sizes (often with dozens to thousands of embryos) in many of the species assayed. The authors of these review articles concluded that the explanation probably has to do not only with the balance between the costs and benefits of multiple mating but also with the finite logistical opportunities for successful mating events during each breeding season or episode.
Depending on the species, constraints on mate acquisition might include ecological and natural-history factors such as low population densities, short mating seasons, poor vagilities, lengthy courtships, and perhaps even post-copulatory phenomena such as sperm competition and cryptic female choice of sperm (Birkhead & Pizzari, 2002; Eberhard, 2009), the net effect being to truncate mate numbers even in animal species with huge broods and high frequencies of polygamy. Such mating-constraint hypotheses can be viewed as null models for reproductive behaviors in nature (Hubbell & Johnson, 1987; Gowaty & Hubbell, 2009), in which case logistical considerations offer a different perspective on mating systems that might help to counterbalance traditional interpretations based on polyandry's purported selective advantages. For example, before invoking a selective explanation for genetic polygamy in any focal species, an important question might be whether the mean number of successful mates per brooder statistically exceeds or does not exceed the suspected rate of mate encounters given each species' particular biology and ecology.