期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2021
卷号：118
期号：35
DOI：10.1073/pnas.2102467118
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Many animals depend on maternally transmitted symbiotic bacteria that provide nutrients or other benefits. The evolution of these symbionts is complicated: natural selection can act on hosts, favoring symbionts that increase host reproduction, or on symbionts, favoring symbionts that spread within hosts. Furthermore, transmission bottlenecks can facilitate the spread of mutations deleterious to both. By measuring changes in frequencies of symbiont genotypes within individual insect matrilines, we estimated within-host selection and transmission bottleneck size. Results revealed surprisingly strong selection, with some symbiont genotypes more successful in colonizing progeny, as well as a severe transmission bottleneck, consistent with observations of deleterious mutation accumulation in symbiont genomes. Findings elucidate the forces driving evolution of heritable symbionts and generating their distinctive genomic features.
Numerous animal lineages have maternally inherited symbionts that are required for host reproduction and growth. Endosymbionts also pose a risk to their hosts because of the mutational decay of their genomes through genetic drift or to selfish mutations that favor symbiont fitness over host fitness. One model for heritable endosymbiosis is the association of aphids with their obligate bacterial symbiont,
Buchnera. We experimentally established heteroplasmic pea aphid matrilines containing pairs of closely related
Buchnera haplotypes and used deep sequencing of diagnostic markers to measure haplotype frequencies in successive host generations. These frequencies were used to estimate the effective population size of
Buchnera within hosts (i.e., the transmission bottleneck size) and the extent of within-host selection. The within-host effective population size was in the range of 10 to 20, indicating a strong potential for genetic drift and fixation of deleterious mutations. Remarkably, closely related haplotypes were subject to strong within-host selection, with selection coefficients as high as 0.5 per aphid generation. In one case, the direction of selection depended on the thermal environment and went in the same direction as between-host selection. In another, a new mutant haplotype had a strong within-host advantage under both environments but had no discernible effect on host-level fitness under laboratory conditions. Thus, within-host selection can be strong, resulting in a rapid fixation of mutations with little impact on host-level fitness. Together, these results show that within-host selection can drive evolution of an obligate symbiont, accelerating sequence evolution.
关键词：enendosymbiosis;within-host selection;levels of selection;mutualism;maternal transmission
