On the evolutionary origins of insect seminal fluid proteins

In most cases, proteins affect the phenotype of the individual in which they are produced. However, in some cases, proteins have evolved in such a way that they are able to influence the phenotype of another individual of the same or of a different species ("influential proteins"). Examples of interspecific influential proteins include venom proteins and proteins produced by parasites that influence their hosts' physiology or behavior. Examples of intraspecific influential proteins include those produced by both mothers and fetuses that mitigate maternal resource allocation and proteins transferred to females in the seminal fluid during mating that change female physiology and behavior. Although there has been much interest in the functions and evolutionary dynamics of these influential proteins, less is known about the origin of these proteins. Where does the DNA that encodes the proteins that can impact another individual's phenotype come from and how do the proteins acquire their influential abilities? In this mini-review, I use insect seminal fluid proteins as a case study to consider the origin of intraspecific influential proteins. The existing data suggest that influential insect seminal fluid proteins arise both through co-option of existing genes (both single copy genes and gene duplicates) and de novo evolution. Other mechanisms for the origin of new insect seminal fluid proteins (e.g., retrotransoposition and horizontal gene transfer) are plausible but have not yet been demonstrated. Additional gaps in our understanding of the origin of insect seminal fluid proteins include an understanding of the cis-regulatory elements that designate expression in the male reproductive tract and of the evolutionary steps by which individual proteins come to depend on other seminal fluid proteins for their activity within the mated female.