From molecules to mating: Rapid evolution and biochemical studies of reproductive proteins

Abstract

Sexual reproduction and the exchange of genetic information are essential biological processes for species across all branches of the tree of life. Over the last four decades, biochemists have continued to identify many of the factors that facilitate reproduction, but the molecular mechanisms that mediate this process continue to elude us. However, a recurring observation in this research has been the rapid evolution of reproductive proteins. In animals, the competing interests of males and females often result in arms race dynamics between pairs of interacting proteins. This phenomenon has been observed in all stages of reproduction, including pheromones, seminal fluid components, and gamete recognition proteins. In this article, we review how the integration of evolutionary theory with biochemical experiments can be used to study interacting reproductive proteins. Examples are included from both model and non-model organisms, and recent studies are highlighted for their use of state-of-the-art genomic and proteomic techniques. Significance Despite decades of research, our understanding of the molecular mechanisms that mediate fertilization remain poorly characterized. To date, molecular evolutionary studies on both model and non-model organisms have provided some of the best inferences to elucidating the molecular underpinnings of animal reproduction. This review article details how biochemical and evolutionary experiments have jointly enhanced the field for 40 years, and how recent work using high-throughput genomic and proteomic techniques have shed additional insights into this crucial biological process.

Co-option and evolution of non-olfactory proteinaceous pheromones in a terrestrial lungless salamander

“…In all molecular and proteomic studies to date, we have demonstrated recruitment and co-option of multiple gene families followed by rapid evolution [23,25,26,28,44]. Specifically, our proteomic studies demonstrate large changes in pheromone composition between genera, even for those using the same delivery mode [28,45]. A key question remains is what factors allow a gene to be coopted.…”

“…This mode of evolution would be similar to that for snake venom TFPs. Maintenance of the multiple SPF isoforms may extend from relaxed purifying selection as a secreted protein that has few interactions with mental gland cytosolic proteins (for thorough review of how gene duplication and sexual selection may affect reproductive protein evolution, see [45]). Interestingly, nearly all of the sequence diversity seems to be due to gene duplication, with an individual D. ocoee mental gland having at least 20 different variants.…”

Fertilization Mechanisms in Flowering Plants

“…mouse and human, clearly demonstrate that species-specific gamete recognition mechanisms are fully in play [47]. Rapidly evolving cell surface proteins play a key role during gamete recognition and adhesion in metazoans and reinforce barriers to interspecific hybridization [48, 49]. We are not equating a pollen tube to a penis here, but the fact that plants have many reproductive hurdles prior to gamete interaction should not be construed to mean that a plant has no species-specific gamete recognition mechanisms.…”

“…Similarly in wind pollinated seed plants the number of sexual male organs (stamens containing anthers) is strongly increased compared to species pollinated by insects [121]. A way in which animal eggs counter sperm onslaught is by rapid diversification of receptors for sperm [48], and by rapid and permanent blocks to polyspermy. The investment made by the egg to blocks to polyspermy in some cases is enormous.…”

Novel seminal fluid proteins in the seed beetle Callosobruchus maculatus identified by a proteomic and transcriptomic approach

“…Sperm competition (Parker, ), the competition between sperm from different males to fertilize the same set of ova, is predicted to be a potent force driving both the evolution of SFPs (Dhole & Servedio, ) and the plasticity of their expression (Fedorka et al ., ; Ramm et al ., ). Indeed, there is now much evidence that SFPs are under positive Darwinian selection (eg Swanson et al ., ; Haerty et al ., ; Ramm et al ., ; for a review of reproductive protein evolution see Wilburn & Swanson, ).…”