Symbiosis as an adaptive process and source of phenotypic complexity

Abstract

Genomics has revealed that inheritance systems of separate species are often not well segregated: genes and capabilities that evolve in one lineage are often stably acquired by another lineage. Although direct gene transfer between species has occurred at some level in all major groups, it appears to be far more frequent in prokaryotes than in multicellular eukaryotes. An alternative to incorporating novel genes into a recipient genome is acquiring a stable, possibly heritable, symbiotic association and thus enjoying benefits of complementary metabolic capabilities. These kinds of symbioses have arisen frequently in animals; for example, many insect groups have diversified on the basis of symbiotic associations acquired early in their evolutionary histories. The resulting associations are highly complex, often involving specialized cell types and organs, developmental mechanisms that ensure transfer of symbionts between generations, and mechanisms for controlling symbiont proliferation and location. The genomes of long-term obligate symbionts often undergo irreversible gene loss and deterioration even as hosts evolve dependence on them. In some cases, animal genomes may have acquired genes from symbionts, mirroring the gene uptake from mitochondrial and plastid genomes. Multiple symbionts often coexist in the same host, resulting in coadaptation among several phylogenetically distant genomes.

Fig. 1.

Schematic diagram of the evolutionary steps in the acquisition of bacterial symbionts and sap-feeding lifestyles in the insect group Auchenorrhyncha (Hemiptera), with emphasis on the sharpshooters (Cicadellinae). The bacterial symbionts S. muelleri (Bacteroidetes) and B. cicadellinicola (Gammaproteobacteria) colonized at different stages in sharpshooter evolution; they provide nutrients needed to supplement the xylem sap diet (–61).

Fig. 2.

An individual sharpshooter (Cuerna sayi) dissected to reveal the brightly colored bacteriomes on each side of the abdomen. These structures contain the intracellular symbionts, Sulcia and Baumannia. Photo by R. Rakitov and D. Takiya, University of Illinois.

Fig. 3.

The two symbionts, Sulcia (red) and Baumannia (green) from the sharpshooter Graphocephala atropunctata. The cells are visualized by using fluorescent in situ hybridization with probes for taxon-specific 16S rRNA sequences (61). The large Sulcia cells are sometimes closely surrounded with Baumannia cells. (Photo by P. Tran and N. Moran, University of Arizona.)