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Ancient host specificity within a single species of brood parasitic bird.

ABSTRACT: Parasites that exploit multiple hosts often experience diversifying selection for host-specific adaptations. This can result in multiple strains of host specialists coexisting within a single parasitic species. A long-standing conundrum is how such sympatric host races can be maintained within a single parasitic species in the face of interbreeding among conspecifics specializing on different hosts. Striking examples are seen in certain avian brood parasites such as cuckoos, many of which show host-specific differentiation in traits such as host egg mimicry. Exploiting a Zambian egg collection amassed over several decades and supplemented by recent fieldwork, we show that the brood parasitic Greater Honeyguide Indicator indicator exhibits host-specific differentiation in both egg size and egg shape. Genetic analysis of honeyguide eggs and chicks show that two highly divergent mitochondrial DNA lineages are associated with ground- and tree-nesting hosts, respectively, indicating perfect fidelity to two mutually exclusive sets of host species for millions of years. Despite their age and apparent adaptive diversification, however, these ancient lineages are not cryptic species; a complete lack of differentiation in nuclear genes shows that mating between individuals reared by different hosts is sufficiently frequent to prevent speciation. These results indicate that host specificity is maternally inherited, that host-specific adaptation among conspecifics can be maintained without reproductive isolation, and that host specificity can be remarkably ancient in evolutionary terms.

SUBMITTER: Spottiswoode CN

PROVIDER: S-EPMC3203796 | biostudies-literature | 2011 Oct

REPOSITORIES: biostudies-literature

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Ancient host specificity within a single species of brood parasitic bird.

Spottiswoode Claire N CN Stryjewski Katherine Faust KF Quader Suhel S Colebrook-Robjent John F R JF Sorenson Michael D MD

Proceedings of the National Academy of Sciences of the United States of America 20110926 43

Parasites that exploit multiple hosts often experience diversifying selection for host-specific adaptations. This can result in multiple strains of host specialists coexisting within a single parasitic species. A long-standing conundrum is how such sympatric host races can be maintained within a single parasitic species in the face of interbreeding among conspecifics specializing on different hosts. Striking examples are seen in certain avian brood parasites such as cuckoos, many of which show h ...[more]

PMID: 21949391

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Project description:Seagrass-dwelling members of the bivalve family Lucinidae harbor environmentally acquired gill endosymbionts. According to previous studies, lucinid symbionts potentially represent multiple strains from a single thioautotrophic gammaproteobacterium species. This study utilized genomic- and transcriptomic-level data to resolve symbiont taxonomic, genetic, and functional diversity from Ctena orbiculata endosymbiont populations inhabiting carbonate-rich sediment at Sugarloaf Key, FL (USA). The sediment had mixed seagrass and calcareous green alga coverage and also was colonized by at least five other lucinid species. Four coexisting, thioautotrophic endosymbiont operational taxonomic units (OTUs), likely representing four strains from two different bacterial species, were identified from C. orbiculata Three of these OTUs also occurred at high relative abundances in the other sympatric lucinid species. Interspecies genetic differences averaged about 5% lower at both pairwise average nucleotide identity and amino acid identity than interstrain differences. Despite these genetic differences, C. orbiculata endosymbionts shared a high number of metabolic functions, including highly expressed thioautotrophy-related genes and a moderately to weakly expressed conserved one-carbon (C1) oxidation gene cluster previously undescribed in lucinid symbionts. Few symbiont- and host-related genes, including those encoding symbiotic sulfurtransferase, host respiratory functions, and host sulfide oxidation functions, were differentially expressed between seagrass- and alga-covered sediment locations. In contrast to previous studies, the identification of multiple endosymbiont taxa within and across C. orbiculata individuals, which were also shared with other sympatric lucinid species, suggests that neither host nor endosymbiont displays strict taxonomic specificity. This necessitates further investigations into the nature and extent of specificity of lucinid hosts and their symbionts.IMPORTANCE Symbiont diversity and host/symbiont functions have been comprehensively profiled for only a few lucinid species. In this work, unprecedented thioautotrophic gill endosymbiont taxonomic diversity was characterized within a Ctena orbiculata population associated with both seagrass- and alga-covered sediments. Endosymbiont metabolisms included known chemosynthetic functions and an additional conserved, previously uncharacterized C1 oxidation pathway. Lucinid-symbiont associations were not species specific because this C. orbiculata population hosted multiple endosymbiont strains and species, and other sympatric lucinid species shared overlapping symbiont 16S rRNA gene diversity profiles with C. orbiculata Our results suggest that lucinid-symbiont association patterns within some host species could be more taxonomically diverse than previously thought. As such, this study highlights the importance of holistic analyses, at the population, community, and even ecosystem levels, in understanding host-microbe association patterns.

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Ancient host specificity within a single species of brood parasitic bird.

Publications

Ancient host specificity within a single species of brood parasitic bird.

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