Viviparity‐driven Conflict

Abstract

Equipped with Mendel's laws and only rudimentary knowledge of genes and genomes, the architects of the Modern Synthesis provided key insights into the dynamics of gene frequency change within populations. Extension of population genetic models to speciation identified Dobzhansky-Muller incompatibilities (negative epistatic interactions between genes from isolated populations) as the primary cause of hybrid inviability and sterility, a view consistent with empirical findings on the genetics of reproductive isolation in Drosophila. Although speciation models have become increasingly mathematically sophisticated, many remain based on an overly static concept of the genome, grounded in Mendelian genetics and devoid of potentially important biological details. A unifying theory of speciation therefore remains elusive, with debate over the relative importance of natural selection, sexual selection, sexual conflict, genetic drift, and selfish genetic elements in the evolution of reproductive isolation. Drawing on recent findings in molecular genetics and comparative genomics, we revisit, update, and extend the theory that reproductive mode plays a crucial role in shaping the speciation process. By providing a direct conduit for manipulation of the mother's physiology by genes expressed in the embryo, viviparity creates a postfertilization arena for genomic conflicts absent in species that lay eggs. In polyandrous species, viviparity-driven conflict (VDC) is likely to generate perpetual antagonistic coevolution between genes expressed during embryonic development and those involved in maternal reproductive physiology, thereby accelerating the rate at which postzygotic isolation evolves between populations. Moreover, in mammals and flowering plants, VDC has favored the evolution of genomic imprinting and a central role for epigenetic mechanisms in the regulation of antagonistic patterns of gene expression by maternally and paternally inherited genomes. VDC can account for the rapid rate at which mammals and viviparous fishes lose their ability to hybridize; the key role of the triploid endosperm in postzygotic reproductive isolation in flowering plants; and the kinds of traits, genes, and gene regulatory systems most critical to the evolution of postzygotic reproductive isolation in live-bearing species.

Diversification and the rate of molecular evolution: no evidence of a link in mammals

“…It has been suggested that hybrid incompatibilities in mammals develop at a much faster rate than in birds [78], possibly due to higher rates of regulatory evolution [78,79]. If reproductive isolation in mammals is determined to a greater degree by adaptive divergence at regulatory and developmental loci (such as those loci associated with placentation, genomic imprinting or mediating viviparity driven conflicts [80-82]), then the molecular change accompanying speciation may be predominantly in a few key loci, rather than due to the accumulation of genome-wide incompatibilities.…”

Life-History Correlates of Placental Structure in Eutherian Evolution

“…Multiple paternity is predicted to promote the evolution of more aggressive paternal genomes (Zeh and Zeh 2000), and since viviparity-driven conflict is predicted to be most intense where genomic-imprinting is most effective (Zeh and Zeh 2008), we may expect a more rapid evolution of postzygotic reproductive barriers in species with more invasive interhemal barriers and particularly high rates of speciation in lineages combining invasive placentation with social systems that allow for multiple paternity. While social organization was not directly tested in this study, the positive association between haemochorial placentation and large group size in our data may be indicative of the effect of social behavior, and polyandry in particular, on the importance of genomic-imprinting in a species.…”

Transposons, environmental changes, and heritable induced phenotypic variability

“…Recently, various reviews and theoretical works have been published which propose a basic hypothesis: Drastic environmental change can disrupt the mechanism of transposon silencing and induce an explosion of transposon activity with the creation of genetic variability. The consequent burst of transpositions could help macroevolutionary processes (Zeh et al 2008; Oliver and Greene 2009; Oliver and Greene 2011; Rebollo et al 2010). This hypothesis, however, has its problems: What little experimental evidence that there is so far shows that, in organisms under stress, there is no direct correlation between the increase in transposon transcripts and the rate of transposition.…”