Ecological and geographical speciation in Lucilia bufonivora: The evolution of amphibian obligate parasitism.

G Arias-Robledo,K Szpila,R Wall,T Whitworth,D Shpeley,T Stark,J.R Stevens,R.A King

doi:10.1016/j.ijppaw.2019.09.005

Abstract

Lucilia (Diptera: Calliphoridae) is a genus of blowflies comprised largely of saprophagous and facultative parasites of livestock. Lucilia bufonivora, however, exhibits a unique form of obligate parasitism of amphibians, typically affecting wild hosts. The evolutionary route by which amphibian myiasis arose, however, is not well understood due to the low phylogenetic resolution in existing nuclear DNA phylogenies. Furthermore, the timing of when specificity for amphibian hosts arose in L. bufonivora is also unknown. In addition, this species was recently reported for the first time in North America (Canada) and, to date, no molecular studies have analysed the evolutionary relationships between individuals from Eastern and Western hemispheres. To provide broader insights into the evolution of the amphibian parasitic life history trait and to estimate when the trait first arose, a time-scaled phylogeny was inferred from a concatenated data set comprising mtDNA, nDNA and non-coding rDNA (COX1, per and ITS2 respectively). Specimens from Canada, the UK, Poland, Switzerland, the Netherlands and Germany were analysed, as well as individuals from its sister taxa, the saprophage Lucilia silvarum and a Nearctic species also implicated in amphibian myiasis, Lucilia elongata. Obligate amphibian parasitism appears to have arisen ~4 mya, likely as a result of niche displacement of a saprophagous/facultative parasite ancestor. Consistent paraphyly of L. bufonivora with respect to L. elongata across single-gene phylogenies and high mtDNA genetic distances between Nearctic and Palearctic individuals suggest on-going cryptic speciation facilitated by geographical isolation. These findings suggest that recent reports of L. bufonivora in the Nearctic do not constitute a recent introduction, but instead suggest that it remained unrecorded due to taxonomic confusion and low abundance. This is the first study to confirm the involvement of L. bufonivora in amphibian myiasis in Canada using DNA-based identification methods.

Highlights

Myiasis is the infestation of a living host, usually vertebrate, with dipterous larvae that feed on the tissues of the host (Zumpt, 1965)
The family Calliphoridae includes a wide range of saprophagous, facultative myiasis agents and a small number of species of obligate parasites (Aubertin, 1933; Zumpt, 1965; Stevens et al, 2006), many of which are of major economic importance in the livestock industry (e.g. Lucilia sericata, Lucilia cuprina, Cochliomyia hominivorax)
The aims of this work were, firstly, to infer the times at which the life history trait of obligate amphibian parasitism arose within a genus that is mainly composed by species with sarco-saprophagous life cycles (Lucilia)

Summary

Introduction

Myiasis is the infestation of a living host, usually vertebrate, with dipterous larvae that feed on the tissues of the host (Zumpt, 1965). Within the super-family Oestroidea, many different lineages of flies are generally recognised as causing myiasis, ranging from highly specific obligate parasites to opportunistic facultative agents of myiasis. Most calliphorid flies typically exhibit low host-specificity, relatively short periods of larval development and are rarely seen infecting hosts in the wild (Zumpt, 1965; Erzinçlioğlu, 1989; Stevens et al, 2006). The toadfly, Lucilia bufonivora, exhibits obligate parasitism for amphibians and is generally associated with wild hosts that rarely survive infestation (Vestjens, 1958; Koskela et al, 1974; Strijbosch, 1980; Gosá et al, 2009; Díaz-Martín et al, 2012).

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