Competitive Dominance among Strains of Luminous Bacteria Provides an Unusual Form of Evidence for Parallel Evolution in Sepiolid Squid-Vibrio Symbioses

Abstract

One of the principal assumptions in symbiosis research is that associated partners have evolved in parallel. We report here experimental evidence for parallel speciation patterns among several partners of the sepiolid squid-luminous bacterial symbioses. Molecular phylogenies for 14 species of host squids were derived from sequences of both the nuclear internal transcribed spacer region and the mitochondrial cytochrome oxidase subunit I; the glyceraldehyde phosphate dehydrogenase locus was sequenced for phylogenetic determinations of 7 strains of bacterial symbionts. Comparisons of trees constructed for each of the three loci revealed a parallel phylogeny between the sepiolids and their respective symbionts. Because both the squids and their bacterial partners can be easily cultured independently in the laboratory, we were able to couple these phylogenetic analyses with experiments to examine the ability of the different symbiont strains to compete with each other during the colonization of one of the host species. Our results not only indicate a pronounced dominance of native symbiont strains over nonnative strains, but also reveal a hierarchy of symbiont competency that reflects the phylogenetic relationships of the partners. For the first time, molecular systematics has been coupled with experimental colonization assays to provide evidence for the existence of parallel speciation among a set of animal-bacterial associations.

The GacA global regulator of Vibrio fischeri is required for normal host tissue responses that limit subsequent bacterial colonization

“…Within hours after hatching, juvenile E. scolopes squid begin to recruit symbionts, offering nutrients in exchange for protective counter-illumination (Nyholm and McFall-Ngai, 2004). It is not known what special attributes set V. fischeri apart from other closely related bacteria that cannot enter into symbiosis, but phylogenetic studies indicate that coevolution has led to impressive specificity (Nishiguchi et al, 1998). Only bacteria that prove they are the correct partner by navigating the gauntlet of host defences (Davidson et al, 2004;Nyholm and McFall-Ngai, 2004), eventually reaching and growing inside the light organ, can induce host-tissue changes, some on the inside of the light organ, and most importantly for this study many on the outer surface of the light organ (Doino and McFall-Ngai, 1995;Nyholm et al, 2002).…”

The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept

“…Interestingly, V. fischeri mutants defective in light production are unable to persist at wild-type levels and, moreover, they are outcompeted by the wild-type V. fischeri (Visick et al, 2000). Even though closely related E. scolopes can become infected by wild-type V. fischeri strains isolated from closely related squid species, the non-native strains are outcompeted when the animals are exposed to their native strain (Nishiguchi et al, 1998). The squid thus selects specific coevolved microorganisms.…”

When can host shifts produce congruent host and parasite phylogenies? A simulation approach

“…phylogenetically more or less distant hosts or the probability of speciation following such a range expansion, remain unclear. Host shifts occur more readily to phylogenetically more similar hosts in several systems (Reed & Hafner, 1997;Janz & Nylin, 1998;Nishiguchi et al, 1998;Ricklefs & Fallon, 2002), but there is no correlation between the phylogenetic distance between host plants and the switches of their leaf beetle parasites (Futuyma et al (1995). Both scenarios of host-switches are plausible: switches will occur preferentially between closely related hosts if the mechanisms employed by a parasite to attack its habitual host are more effective on a closely related host or if closely related hosts have more similar habitat requirements.…”