Paradox of Mother's Curse and the Maternally Provisioned Offspring Microbiome

Strict maternal transmission creates an “asymmetric sieve” favoring the spread of mutations in organelle genomes that increase female fitness, but diminish male fitness. This phenomenon, called “Mother''s Curse,” can be viewed as an asymmetrical case of intralocus sexual conflict. The evolutionary logic of Mother''s Curse applies to each member of the offspring microbiome, the community of maternally provisioned microbes, believed to number in the hundreds, if not thousands, of species for host vertebrates, including humans. Taken together, these observations pose a compelling evolutionary paradox: How has maternal transmission of an offspring microbiome become a near universal characteristic of the animal kingdom when the genome of each member of that community poses a potential evolutionary threat to the fitness of host males? I review features that limit or reverse Mother''s Curse and contribute to resolving this paradox. I suggest that the evolution of vertical symbiont transmission requires conditions that mitigate the evolutionary threat to host males.The genomes of mitochondria, chloroplasts, and many symbiotic microbes are transmitted maternally by host females to their offspring. Maternal transmission can be transovariole (intracellular, within the egg) or contagious, during gestation, birth, or feeding (Sonneborn 1950; Smith and Dunn 1991; Gillham 1994; O’Neill et al. 1997). Vertically transmitted (VT) symbiont lineages tend to be genetically homogeneous within hosts (Birky et al. 1983, 1989; Funk et al. 2000). Maternal uniparental transmission creates an “asymmetric sieve” wherein mutations advantageous for females, but harmful for males, can spread through a population (Cosmides and Tooby 1981; Frank and Hurst 1996; Zeh and Zeh 2005; Burt and Trivers 2006). Such mutations spread because deleterious male-specific fitness effects do not affect the response to natural selection of the maternally transmitted entities. This adaptive process favoring the transmitting sex is called Mother''s Curse (MC) (Gemmell et al. 2004) and it has been referred to as an irreconcilable instance of intralocus conflict: “… exclusively maternal transmission of cytoplasmic genes (e.g., in mitochondria) can result in suboptimal mitochondrial function in males … a form of intralocus sexual conflict] that apparently cannot be resolved, because selection on mitochondria in males cannot produce a response” (Bonduriansky and Chenoweth 2009, p. 285).Mitochondria are ubiquitous in animals and despite the indisputable evolutionary logic of MC (Frank and Hurst 1996) there are no reported cases of sperm-killing or son-killing mitochondria (Burt and Trivers 2006). Moreover, many species of animals possess an offspring microbiome, a community of microbes transmitted uniparentally from mother to offspring at some point in development, whether prefertilization, postfertilization, or postnatal (Funkhouser and Bordenstein 2013). In some vertebrates, including humans, this community is believed to number in the hundreds of species (Funkhouser and Bordenstein 2013). Prolonged periods of maternal care, as in mammals and birds, as well as kin-structured sociality, afford many opportunities for maternal provisioning of microbes to developing offspring. The social insects, in particular, show obligate mutualisms with a microbiome that confers important nutritional benefits for its host (Baumann 2005; Engel and Moran 2013), the termites being a classic example (Ikeda-Ohtsubo and Brune 2009).Together, the evolutionary logic of MC and the widespread existence of maternally transmitted hereditary symbioses pose a paradox for evolutionary biology. The maternally provisioned microbiome (MC) consists of tens to hundreds of genomes affording ample opportunity, along with mitochondrial and organelle genomes, for the occurrence of mutations that benefit females while harming host males. Assembling a VT community as a host nutritional or defensive adaptation requires evading MC not once, but from a continuous siege over evolutionary time. This is the Mother''s Curse–microbiome (MC–MB) paradox. It conceptually affiliated with the “paradox of mutualism,” the persistence of interspecific mutualisms despite the advantages of cheating by one or the other member of the mutualism (Heath and Stinchcombe 2014). Symbiont “cheating” on only half the members of a host species, the males, might offer marginal benefits relative to wholesale cheating on both host sexes. Nevertheless, the MC–MB paradox deserves research attention.In this review, I discuss inbreeding, kin selection, compensatory evolution, and defensive advantages against more virulent pathogens (or predators and herbivores) as means for resolving the MC–MB paradox. First, I review the simple population genetics of MC. I discuss how host inbreeding and kin selection (Unckless and Herren 2009; Wade and Brandvain 2009), alone or in concert, allow for a response to selection on male fertility and viability fitness effects of maternally transmitted genomes. As a result, inbreeding and kin selection can limit or prevent the spread of mutations in a hereditary symbiosis (Cowles 1915) that are harmful to males. I will show that, for both inbreeding and kin selection, there exist conditions that “favor the spread of maternally transmitted mutations harmful to females”; a situation that is the reverse of MC. However, many outbreeding, asocial species harbor maternally provisioned microbiomes and these solutions cannot be applied to them.I also consider the evolution of compensatory nuclear mutations that mitigate or eliminate the harm to males of organelles or symbionts, spreading via MC dynamics. However, I find that the relative rate of compensatory evolution is only 1/4 the rate of evolution of male-harming symbionts. Thus, an evolutionary rescue of host males via compensatory host nuclear mutations requires that there be fourfold or more opportunities for compensation offered by a larger host nuclear genome. The larger the number of species in a host microbiome, the more difficult it is to entertain host nuclear compensatory mutations as a resolution of the MC–MB paradox.Next, I consider the situation in which a deleterious, VT symbiont harms its host but prevents host infection by a more severely deleterious contagiously transmitted pathogen (Lively et al. 2005; see also Clay 1988). This is a case in which absolute harm to a host by a maternally provisioned symbiont becomes a “relative” fitness advantage. This is a scenario that may be common in hosts with speciose microbial communities, especially if each microbial species increases host resistance or outright immunity to infectious, virulent pathogens.Finally, I discuss models of symbiont domestication and capture via the evolution of vertical transmission from an ancestral state of horizontal transmission (Drown et al. 2013). I show that the evolution of vertical transmission requires conditions that tend to restrict the capacity for male harming by symbionts. Each of these scenarios significantly expands the range of evolutionary possibilities permitted for the coevolution of host–symbiont assemblages, especially those microbial communities that are maternally, uniparentally transmitted across host generations. Unfortunately, current data do not permit discriminating among these various evolutionary responses to MC, so none can be definitively considered a resolution of the MC–MB paradox.