Studies of animal fertilization proteins have focused on species with separate sexes, in which self-fertilization, or selfing, cannot occur. In hermaphrodites it is unclear how an animal avoids fertilizing its own eggs with its own sperm, in other words, how it achieves self-incompatibility. The goal of this proposal is to characterize the evolutionary forces that govern genetic variation in self-incompatibility genes in the invasive ascidian, Ciona intestinalis. Understanding self-incompatibility has profound implications for understanding mate recognition in general. The self-incompatibility (SI) loci in C. intestinalis are the first definitive SI loci to be characterized in animals. This research will be among the first to elucidate how animals have responded to the challenges of avoiding inbreeding, and balancing fitness from male and female gametes. This research will also build upon an extensive body of work on the role of mate availability as an evolutionary force in marine systems.
Invasive species cost the U.S. about $120 billion/year and have devastating effects on ecosystem diversity. Ciona contributes to these costs by contaminating aquaculture projects, fouling boats, and outcompeting native species. Evidence from invasive plants suggests that changes in the prevalence of selfing may facilitate invasion success. Identification of selfing genotypes could reveal populations with greater potential for invasion and range expansion.
All sexually reproducing organisms face the challenge of avoiding matings with close relatives (inbreeding), and the associated costs of reduced vigor of young. Hermaphroditic organisms face the most extreme challenge of all, namely avoiding the possibility of self-fertilization. Some animals limit inbreeding by actively avoiding mating with kin. However, virtually all flowering plants (and many aquatic organisms) depend on either wind, water, or pollinators (insects, birds, and bats) to transport sperm to eggs (or pollen to ovules), and lack direct control over fertilization. Consequently, many plants have evolved genetic barriers to self-fertilization, embodied in what are known as self-incompability (SI) systems. In such systems, individuals that are too genetically similar cannot fertilize each other, as would be the case in either a self-pollination, or a pollination involving close relatives. This barrier to selfing and inbreeding produces a form of natural selection that favors rare genetic variants, and is called negative frequency-dependent selection. The outcome of this form of selection is the maintenance of extraordinary levels of genetic variation in natural populations of many plants. Virtually nothing is known about whether such systems exist in hermaphroditic aquatic animals, and the genetics underlying SI. This project focused on a marine sea squirt (a chordate, like ourselves), Ciona intestinalis A, that is invading harbors throughout the world, and causing substantial economic damage by fouling piers, pilings and boats. We sequenced the genes that are candidates for the control of fertilization in this sea squirt. We found that the genes belong to a complex and very rapidly evolving gene family, and that the copies of the gene expressed in sperm and egg appear to be evolving antagonistically. We were also able to identify, through population genomic analyses, which parts of the genes were experiencing the strongest selection. Finally, we have been able to use these variable SI genes to to track the spread of this invasive species across the harbors and waterways of the coastal oceans in the northern and southern hemispheres. By identifying such pathways in this species, and others with similar properties, it will be easier to develop remediation programs to limit their spread. The project supported the completion of the doctoral dissertation of one female Ph.D. student, and provided training in modern genetic and genomic analyses to 3 undergraduate women, two of whom belong to under-represented groups in STEM disciplines.
