The phylogeny of the nematode family Metastrongylidae Leiper, [1909]: a correlation of host and symbiote evolution

Abstract

1. History of the classification of the family Metastrongylidae is briefly reviewed.2. The probable origin of the family is discussed. It is believed that the metastrongylids arose, in common with the family Strongylidae, from a primitive group of eustomatous, cloacinin-like, gastro-intestinal strongylines that were symbiotic with an ancestral mammalian group, possibly the pantotheres. One group of these symbiotes established itself in the mammalian respiratory tract and originated the metastrongylid line.3. The family Trichostrongylidae is regarded as of common origin with the family Ancylostomatidae from eustomatous ancestors. Thus meiostomy in the metastrongylids and trichostrongylids is convergent.4. The Metastrongylidae consist of three main lines, each characteristic of a placentate order: the Filaroidinae in the Carnivora, the Pseudaliinae in the Cetacea, and the Protostrongylinae in the Artiodactyla. These lines probably have evolved from a common ancestor, symbiotic with a host at the base of the carnivore-cetacean-ariodactyl radiation. Certain forms have become secondarily adapted to symbiosis with members of other placentate orders.5. Morphological and biological evidence is given for each of the foregoing phylogenetic conclusions.6. Metastrongylus Molin, 1861, is regarded as a relict genus. With it, in a subfamily Metastrongy-linae, is placed the genus Heterostrongylus Travassos, 1925.7. Heterostrongylus is represented by a single known species, H. heterostrongylus Travassos, 1925, from an opossum (order Marsupialia). Morphologically it is primitive with cloacinin-like cephalic features. In view of the phylogenetic status of its host it may well represent an ancestral type that has evolved along with the Marsupialia from a common ancestry with the other metastrongylids, probably in the panthotheres. As yet unknown lungworms of marsupials may shed light on this interesting point.8. Diagnoses are given for the family Metastrongylidae and its subfamilies; the twenty-two component genera are listed under the latter. New synonymies are made: Neometastrongylus Kreis, 1944, a synonym of Neostrongylus Gebauer, 1932; Neometastrongylus buechii Kreis, 1944, of Neostrongylus linearis (Marotel, 1913) Gebauer, 1932; and Otophocaenurus Skriabin, 1942, of Pharurus Leuckart, 1848. Otophocaenurus oserskoi Skriabin, 1942, becomes Pharurus oserskaiaae (Skriabin, 1942, n.emend.) n.comb.; Metathelazia massino becomes M. massinoi (Davtian in Skriabin, 1933, n.emend.) Dougherty, 1943.

The mitochondrial genome of Protostrongylus rufescens – implications for population and systematic studies

“…In addition, there has been considerable debate as to the relationships among suborders within the Strongylida, based on the use of phenotypic characters [42]. On one hand, it has been hypothesized that the suborder Metastrongylina (to which species of Protostrongylus , Metastrongylus , Aelurostrongylus and Angiostrongylus belong) originated from ancestors in the Strongylina [43,44] or Trichostrongylina [45,46]. On the other hand, it has been proposed that the Metastrongylina gave rise to the Strongylina [47].…”

Evolutionary Relationships among the Protostrongylidae (Nematoda: Metastrongyloidea) as Inferred from Morphological Characters, with Consideration of Parasite-Host Coevolution

“…Furthermore, members of this genus occur exclusively in suids and use earthworms as intermediate hosts rather than gastropods as in most other groups including the Protostrongylidae. These features provide sufficient evidence that Metastrongylidae is distinct from other groups, and it is generally believed to be basal to the other major families in the Metastrongyloidea (Dougherty, 1949;Lichtenfels, 1987;Durette-Desset et al, 1994). Consequently, based on this justification, Metastrongylidae and Metastrongylus apri, respectively, were designated as outgroups for hierarchical analysis of genera and species of Protostrongylidae in the present study.…”

“…Varestrongylus alpenae from the lungs of the white-tailed deer Odocoileus virginianus Zimmermann was originally described as a species of Pneumostrongylus. Similarly, P. tenuis was originally described by Dougherty (1945) ., 1994). Members of the metastrongyloid Skrjabingylidae parasitize the sinuses of mustelids.…”

“…Although the Metastrongyloidea are presently unresolved, there is substantial evidence that the Metastrongylidae (and species of Metastrongylus Molin, 1861) are basal in the superfamily. Species of Metastrongylus have well developed cephalic labia, a simple guberaculum (sometimes absent), and a unique structure for bursal rays (Dougherty, 1949). Additionally, they are oviparous and the egg-shell is thick (Anderson, 1978).…”

“…Within the Metastrongyloidea, the Protostrongylidae were believed by Dougherty (1949) to be part of a lineage that included the Filaroidinae and Pseudaliinae. He suggested that these 3 lineages corresponded, respectively, to radiations in carnivores, cetaceans, and artiodactyles.…”