Evolution of modes of nutrient absorption in entomoparasitic nematodes of the order Tylenchida revealed by structural and phylogenetic analysis

Abstract

Summary Adult female entomoparasitic nematodes of the order Tylenchida have degenerate digestive organs and body surfaces that lack cuticles and are covered with microvilli. These morphologic features indicate that tylenchids absorb nutrients via the integument. A previous study hypothesised that the nutrient intake of entomoparasitic tylenchids evolved from oral to transdermal in a step-by-step manner, and this evolutionary process is reflected in the development of the integument ultrastructure of these species. However, the evolution of the nutrient absorption of entomoparasitic tylenchids remains unclear. This evolution has not been phylogenetically examined because of a lack of information on the integument structure associated with phylogenetic relationships. In the present study, we examined the integument ultrastructure and molecular sequence of four entomoparasitic tylenchids: Bradynema sp., Contortylenchus sp., C. genitalicola and Deladenus sp. The body surface of Bradynema sp. was covered with microvilli, suggesting that Bradynema sp. absorbs nutrients via the integument. By contrast, the body surfaces of Contortylenchus sp., C. genitalicola and Deladenus sp. were covered with a thin cuticle-like layer and well-developed epidermis without microvilli, suggesting that these species absorb nutrients only partially via the integument. We also classified the nutrient absorption mode based on the integument ultrastructure and molecular phylogenetic analysis of entomoparasitic tylenchids in previous studies. Our maximum parsimony analysis supported the step-by-step evolution hypothesised in the previous study. However, the parsimony analysis also generated new evolutionary processes in which atavism and/or saltation occur instead of stepwise evolution.