Reproductive Character Displacement and the Genetics of Gamete Recognition in Tropical Sea Urchins

Abstract

Reproductive character displacement occurs when sympatric and allopatric populations of a species differ in traits crucial to reproduction, and it is commonly thought of as a signal of selection acting to limit hybridization. Most documented cases of reproductive character displacement involve characters that are poorly understood at the genetic level, and rejecting alternative hypotheses for biogeographic shifts in reproductive traits is often very difficult. In sea urchins, the gamete recognition protein bindin evolves under positive selection when species are broadly sympatric, suggesting character displacement may be operating in this system. We sampled sympatric and allopatric populations of two species in the sea urchin genus Echinometra for variation in bindin and for the mitochondrial cytochrome oxidase I to examine patterns of population differentiation and molecular evolution at a reproductive gene. We found a major shift in bindin alleles between central Pacific (allopatric) and western Pacific (sympatric) populations of E. oblonga. Allopatric populations of E. oblonga are polyphyletic with E. sp. C at bindin, whereas sympatric populations of the two species are reciprocally monophyletic. There is a strong signal of positive selection (P N /P S ϭ 4.5) in the variable region of the first exon of bindin, which is associated with alleles found in sympatric populations of E. oblonga. These results indicate that there is a strong pattern of reproductive character displacement between E. oblonga and E. sp. C and that the divergence is driven by selection. There is much higher population structure in sympatric populations at the bindin locus than at the neutral mitochondrial locus, but this difference is not seen in allopatric populations. These data suggest a pattern of speciation driven by selection for local gamete coevolution as a result of interactions between sympatric species. Although this pattern is highly suggestive of speciation by reinforcement, further research into hybrid fitness and egg-sperm interactions is required to address this potential mechanism for character displacement.

Comparative Analysis of Testis Protein Evolution in Rodents

“…In marine invertebrates, through a combination of detailed analysis of evolutionary patterns within and between recently diverged species and functional characterization of positively selected genes, great progress has been made in identifying the selective forces promoting divergence of sperm proteins (Geyer and Palumbi 2003;Levitan and Ferrell 2006;Riginos et al 2006) and determining the consequences of protein divergence on fertilization potential between species (Lyon and Vacquier 1999;Palumbi 1999;Levitan and Ferrell 2006). In mammals, however, a detailed understanding of the causes and consequences of the rapid divergence of reproductive proteins remains elusive (Turner and Hoekstra 2008b).…”

Speciation and the evolution of gamete recognition genes: pattern and process

“…In areas where it lives in sympatry with a closely related (as yet unnamed) species Echinometra species C, the bindin alleles of E. oblonga are divergent from those of allopatric E. oblonga populations, and show a signal of positive selection (Geyer and Palumbi, 2003). The combination of divergence in sympatry and positive selection suggests the action of reinforcement, which might be acting to fix mutations in gamete recognition loci among coexisting species that can prevent fertilization.…”

“…These mechanisms can be species specific or quite general among taxa (Vieira and Miller, 2006). Because basic fertilization demands the interaction of proteins produced by male and female genomes, it can be driven by evolutionary pressures that act on mating systems such as gender conflict (Gavrilets and Waxman, 2002;Gavrilets and Hayashi, 2005;Tomaiuolo et al, 2007), reinforcement (Geyer and Palumbi, 2003) or other aspects of the evolution of reproductive isolation (Tomaiuolo et al, 2007). Because gamete recognition involves relatively few gene products, as opposed to more complex mating barriers in fish and many terrestrial animals, the evolutionary pressures that act to cause reproductive isolation may be more obvious in these simple genetic systems (Palumbi, 1992).…”

Proteomics enhances evolutionary and functional analysis of reproductive proteins

“…In these circumstances, selection could act to prevent hybridization by causing divergence in reproductive characters. (88,89) A fourth hypothesis is that reproductive proteins evolve to avoid pathogens: if gametes, nutrient-rich eggs in particular, are subject to pathogen attack during development, spawning, ovulation, or fertilization, their surface proteins may evolve rapidly to avoid this cost. If changes to inhibit pathogen entry make sperm entry more difficult, then sperm must coevolve with the egg to maintain fertilization compatibility.…”