Resource-associated Population Subdivision in a Symbiotic Coral-reef Shrimp.

The importance of sympatric speciation remains controversial. An empirical observation frequently offered in its support is the occurrence of sister taxa living in sympatry but using different resources. To examine the possibility of sympatric differentiation in producing such cases, I measured genetic, behavioral, and demographic differentiation between populations of the tropical sponge-dwelling shrimp Synalpheus brooksi occupying two alternate host species on three reefs in Caribbean Panama. This species belongs to an apparently monophyletic group of ≥ 30 species of mostly obligate, host-specific sponge-dwellers, many of which occur in sympatry. Demographic data demonstrated the potential for disruptive selection imposed by the two host species: shrimp demes from the sponge Agelas clathrodes were consistently denser, poorer in mature females, more heavily parasitized by branchial bopyrid isopods, and less parasitized by thoracic isopods, than conspecific shrimp from the sponge Spheciospongia vesparium. Laboratory assays demonstrated divergence in host preference: shrimp on all three reefs tended to choose their native sponge species more often than did conspecific shrimp from the other host. Because S. brooksi mates within the host, this habitat selection should foster assortative mating by host species. A hierarchical survey of protein-electrophoretic variation also supported host-mediated divergence, revealing the following: (1) shrimp from the two hosts are conspecific, as evidenced by absence of fixed allelic differences at any of nine allozyme loci scored; (2) strong genetic subdivision among populations of this philopatric shrimp on reefs separated by 1-3 km; and (3) significant host-associated genetic differentiation within two of the three reefs. Finally, intersexual aggression (a proxy for mating incompatibility) between shrimp from different host species was significantly elevated on the one reef where host-associated genetic differences were strongest, demonstrating concordance between genetic and behavioral estimates of divergence. Adjacent reefs appear to be semi-independent sites of host-associated differentiation, as evidenced by differences in the degree of host-associated behavioral and genetic differentiation, and in the specific loci involved, on different reefs. In philopatric organisms with highly subdivided populations, such as S. brooksi, resource-associated differentiation can occur independently in different populations, thus providing multiple "experiments" in differentiation and resulting in a mosaic pattern of polymorphism as reflected by neutral genetic markers. Several freshwater fishes, an amphipod, and a snail similarly show independent but remarkably convergent patterns of resource-associated divergence in different conspecific populations, often in the absence of obvious spatial barriers. In each case, substantial differentiation has occurred in the face of continuing gene flow.