Some assembly required: evolutionary and systems perspectives on the mammalian reproductive system

Abstract

In this review, we discuss the way that insights from evolutionary theory and systems biology shed light on form and function in mammalian reproductive systems. In the first part of the review, we contrast the rapid evolution seen in some reproductive genes with the generally conservative nature of development. We discuss directional selection and coevolution as potential drivers of rapid evolution in sperm and egg proteins. Such rapid change is very different from the highly conservative nature of later embryo development. However, it is not unique, as some regions of the sex chromosomes also show elevated rates of evolutionary change. To explain these contradictory trends, we argue that it is not reproductive functions per se that induce rapid evolution. Rather, it is the fact that biotic interactions, such as speciation events and sexual conflict, have no evolutionary endpoint and hence can drive continuous evolutionary changes. Returning to the question of sex chromosome evolution, we discuss the way that recent advances in evolutionary genomics and systems biology and, in particular, the development of a theory of gene balance provide a better understanding of the evolutionary patterns seen on these chromosomes. We end the review with a discussion of a surprising and incompletely understood phenomenon observed in early embryos: namely the Warburg effect, whereby glucose is fermented to lactate and alanine rather than respired to carbon dioxide. We argue that evolutionary insights, from both yeasts and tumor cells, help to explain the Warburg effect, and that new metabolic modeling approaches are useful in assessing the potential sources of the effect.

Proteomic and evolutionary analyses of sperm activation identify uncharacterized genes in Caenorhabditis nematodes

“…Overall, our findings of sequence conservation over such long evolutionary time periods are contrary to observations within many other organisms, where elevated signals of positive selection are detected in seminal fluid proteins [ 33 – 35 ]. From an evolutionary perspective, then, patterns of evolution in secreted membranous organelle proteins do not match expectations for typical seminal fluid proteins.…”

Exploring the Diversity of Plant Metabolism

“…additionally highlight fascinating observations that aspects of the latter are conserved across the kingdoms of life [22], and that the Crabtree and Warburg effects of yeast and cancer cells, respectively, harbor considerable metabolic similarities [75,76], suggesting that the drive for efficient functionality means that convergent evolution has an amazingly broad scope. Staying at the general level, a recent modeling study evaluated E. coli metabolism with regard to what the authors refer to as 'diversity-generating biosynthesis', which they postulate evolved to produce large numbers of different metabolites [77].…”

Rapid Gene Family Evolution of a Nematode Sperm Protein Despite Sequence Hyper-conservation

“…However, the dynamics of the latter case are predominantly driven by molecular interactions, as opposed to behavioral ones, and therefore the appropriate unit of evolutionary analysis is the molecular evolution of the reproductive proteome ( McDonough et al 2016 ; Wilburn and Swanson 2016 ). Studies across a wide range of vertebrate and invertebrate taxa have consistently shown that reproductive proteins have an elevated ratio of nonsynonymous to synonymous substitutions relative to nonreproductive proteins ( Swanson and Vacquier 2002 ; Clark et al 2006 ; Vacquier and Swanson 2011 ; Mordhorst et al 2015 ). In fact, sperm-specific, seminal fluid, and egg-specific proteins evolve at astonishingly rapid rates, and are often the fastest observed within a given genome.…”