Sea urchin gamete incompatibility

Sea urchins have been a workhorse model for research on animal fertilization for more than a century.  Evolutionary biologists became interested in this work when reports of rapid evolution of barriers to fertilization between species, and rapid adaptive divergence of sperm bindin was found between species in the genus Echinometra in the Indo-West Pacific, and in several other genera.  Bindin is the protein that sea urchin sperm uses to adhere  to egg surfaces prior to sperm-egg fusion, and this step is known to control species specific fertilization.  Together, this suggests that bindin controls gamete recognition between species, and that its evolutionary divergence may play a role in the emergence of reproductive isolation during marine speciation.

My work with Haris Lessios on the three species of Echinometra in Panamá (photos above) also revealed rapid evolution of gamete incompatibility.  Here we were able to show that this process much more recently than the closure of the central American Isthmus (about 3 million years ago).  But fertilization barriers evolve episodically, being strong in the tropical Atlantic species Echinometra lucunter, but weak in the Caribbean E. viridis and just about absent in the Pacific E. vanbrunti.  We showed that the strength of positive selection on sperm bindin exactly mirrors this pattern across species—strong in E. lucunter and absent in the other two species.  This shows that adaptive divergence of bindin evolves in parallel with gamete incompatibility and is strong evidence that the two are linked, but it also suggests a need to understand why this evolutionary process is episodic, and why it proceeds at different rates in different species.

My lab is interested in understanding the forces operating between and within species that drive the evolution of fertilization barriers and promote positive selection on bindin and other gamete recognition proteins.  Progress in this research will require understanding how gamete recognition protein evolution is influenced by conditions in natural populations of spawning animals.  Work in that direction is in progress, in collaboration with Phil Yund and postdoc Anna Bass.  We are using experiments in laboratory flumes (photo below), using the green urchin Strongylocentrotus droebachiensis to study how bindin genotype effects a male's fertilization success in sperm competition, and how the outcome  is influenced by flow conditions around spawning urchins.

Evolution of gamete incompatibility in hybridizing blue mussels

Sea urchins offer a number of advantages for studying the evolution of gamete incompatibility.  In particular, 100 years of research on the mechanisms of fertilization provide a framework that is not available in other species.  But there is a drawback, and that is that hybrids are rarely found in natural populations of sea urchins, even in species between which crosses yield compatible fertilizations.  This questions whether gametic barriers help initiate speciation; they may appear after species are separated for other reasons.  It also suggests that postzygotic barriers must also contribute to maintaining species boundaries in present-day populations.

Blue mussels offer an alternative system in which to study the evolution of gamete incompatibility in an earlier stage of the speciation process—when reproductive isolation is only partially complete, and populations come into secondary contact.  Populations in Cobscook Bay Maine (above, right) and throughout the Canadian Maritimes contain a mixture of two species, Mytilus edulis and M. trossulus, with hybrids between the two accounting for ³ 15% of the population.  Our colleagues and we have shown that gamete incompatibility between these species is strong but highly variable.  Egss from some M. edulis females are are completely blocked to heterospecific fertilization, whereas other females are well fertilized by M. trossulus sperm at the same sperm concentrations.  This partial barrier may help account for the pattern of hybridization in natural populations, and it offers opportunities to study the factors that affect the evolution of gametic isolation in a case where speciation is still "in progress."

Our work combines studies of fertilization and other gamete interactions, of the genetics of the hybrid zone, and of the molecular evolution of sperm lysins, putative gamete recognition proteins in Mytilus.  Some of our recent interest has centered on the study of reproductive character displacement, on patterns of lysin introgression, and most recently on the role of polyspermy avoidance.

Assortative mating and genetic differentiation in a coral reef fish species flock

Coral reef fish are the most speciose of all vertebrate groups, and display a spectacular diversity of coloration and color pattern, even between apparently closely related species.  We know from work on the famous cichlid species flocks, and from other animals, that color pattern and mate preferences based on color can both evolve very rapidly.  Is color pattern based assortative mating an engine in speciation in coral reef fishes?  This question has motivated our interest in the hamlets of the Caribbean.

Hamlets are small seabasses, genus Hypoplectrus, of which about a dozen forms exist in the Caribbean.  Most have been described as species based entirely upon their vivid color pattern differences.  Very little or no other morphological differences exist between species.