Under pressure: phenotypic divergence and convergence associated with microhabitat adaptations in Triatominae

Parasites & Vectors

M. Dolores Bargues¹  Santiago Mas-Coma¹  M. Ángeles Zuriaga¹  Charles B. Beard²  Marcelo Aguilar³  James S. Patterson⁴  Michael A. Miles⁴  Fernando A. Monteiro⁵  Márcio G. Pavan⁶  Fernando Abad-Franch⁷ 

[1] Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Valencia, Spain;Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, USA;Facultad de Ciencias Médicas, Universidad Central del Ecuador, Quito, Ecuador;Instituto Juan César García, Quito, Ecuador;Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK;Laboratório de Epidemiologia e Sistemática Molecular, Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, Brazil;Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, USA;Laboratório de Mosquitos Transmissores de Hematozoários, Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, Brazil;Núcleo de Medicina Tropical, Faculdade de Medicina, Universidade de Brasília, Brasília, Brazil;Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK;

关键词: Triatominae;    Rhodnius;    Chagas disease;    Systematics;    Morphometrics;    Genetics;   

DOI  :  10.1186/s13071-021-04647-z

来源: Springer

【 摘 要 】

BackgroundTriatomine bugs, the vectors of Chagas disease, associate with vertebrate hosts in highly diverse ecotopes. It has been proposed that occupation of new microhabitats may trigger selection for distinct phenotypic variants in these blood-sucking bugs. Although understanding phenotypic variation is key to the study of adaptive evolution and central to phenotype-based taxonomy, the drivers of phenotypic change and diversity in triatomines remain poorly understood.Methods/resultsWe combined a detailed phenotypic appraisal (including morphology and morphometrics) with mitochondrial cytb and nuclear ITS2 DNA sequence analyses to study Rhodnius ecuadoriensis populations from across the species’ range. We found three major, naked-eye phenotypic variants. Southern-Andean bugs primarily from vertebrate-nest microhabitats (Ecuador/Peru) are typical, light-colored, small bugs with short heads/wings. Northern-Andean bugs from wet-forest palms (Ecuador) are dark, large bugs with long heads/wings. Finally, northern-lowland bugs primarily from dry-forest palms (Ecuador) are light-colored and medium-sized. Wing and (size-free) head shapes are similar across Ecuadorian populations, regardless of habitat or phenotype, but distinct in Peruvian bugs. Bayesian phylogenetic and multispecies-coalescent DNA sequence analyses strongly suggest that Ecuadorian and Peruvian populations are two independently evolving lineages, with little within-lineage phylogeographic structuring or differentiation.ConclusionsWe report sharp naked-eye phenotypic divergence of genetically similar Ecuadorian R. ecuadoriensis (nest-dwelling southern-Andean vs palm-dwelling northern bugs; and palm-dwelling Andean vs lowland), and sharp naked-eye phenotypic similarity of typical, yet genetically distinct, southern-Andean bugs primarily from vertebrate-nest (but not palm) microhabitats. This remarkable phenotypic diversity within a single nominal species likely stems from microhabitat adaptations possibly involving predator-driven selection (yielding substrate-matching camouflage coloration) and a shift from palm-crown to vertebrate-nest microhabitats (yielding smaller bodies and shorter and stouter heads). These findings shed new light on the origins of phenotypic diversity in triatomines, warn against excess reliance on phenotype-based triatomine-bug taxonomy, and confirm the Triatominae as an informative model system for the study of phenotypic change under ecological pressure.

【 授权许可】

CC BY