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Fossil evidence of phorid parasitism (Diptera: Phoridae) by allantonematid nematodes (Tylenchida: Allantonematidae)

Published online by Cambridge University Press:  05 December 2003

G. POINAR
G. POINAR
Affiliation:
Department of Zoology, Oregon State University, Corvallis, Oregon 97331, USA
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Abstract

Howardula helenoschini sp. n. (Tylenchida: Allantonematidae) is described from 40 million year-old Baltic amber. The nematodes are parasitic in the body cavity of an adult fly of the genus Triphleba (Phoridae: Diptera). Characteristics of the fossil species are the large size of the pre-adult juveniles and a small number of progeny compared with extant Howardula parasites of flies. Reasons are given why these features suggest that this species was at an early stage of adapting, evolutionarily, to its insect host.

Keywords

fossil nematodesscuttle fly parasitesBaltic amber

Information

Type
Research Article
Information
Parasitology , Volume 127 , Issue 6 , December 2003 , pp. 589 - 592
Copyright
2003 Cambridge University Press

INTRODUCTION

Fossil evidence of nematode parasitism is rare, with most reports confined to insect hosts in amber (Poinar, 1992, 2001). The present study describes a new species of Howardula (Allantonematidae: Tylenchida) from a member of the family Phoridae (Diptera) in Baltic amber. This is the first fossil record of nematode parasitism of a member of the family Phoridae and the earliest fossil record of the Allantonematidae. Previous reports of fossil allantonematids parasitizing drosophilid flies (Poinar, 1984) and staphylinid beetles (Poinar & Brodzinsky, 1986) were in younger Dominican amber. Baltic amber has been dated at approximately 40 million years (Poinar, 1992).

MATERIALS AND METHODS

The amber piece was re-polished to obtain a better view of the nematodes. The final piece weighed 0·2 grams, was 18 mm in greatest length, 6 mm in greatest width and 3 mm in greatest depth. Observations, drawings and photographs were made with a Nikon SMZ-10 stereoscopic microscope and Nikon Optiphot microscope (with magnifications up to 650×). The piece of amber containing the nematodes and fly host is deposited in the Poinar amber collection, maintained at Oregon State University (Acc. # N-3-64).

RESULTS

In the amber are 5 nematodes clustered at the posterior tip of the phorid fly. All 5 nematodes are roughly the same size. However, due to their position, only 2 could be measured and examined in detail. In addition to these stages in the amber, a lemon-shaped body in the abdomen of the fly (best seen with transmitted light) was interpreted to represent the parasitic female nematode. The 2 nematodes that could be studied in detail (specimens A and B) were both determined to be adults within cast juvenile cuticles and, on the basis of morphological characters, were assigned to the genus Howardula. Specimen A, which lacked a stylet and vulva but had a well-defined cloacal opening and the suggestion of spicules, was interpreted to be a male while specimen B, which possessed a stylet and vulva, as well as tissue (presumably ovarian) extending anteriorly from the vulvar region, was considered a female. Members of the genus Howardula are unique in the family Allantonematidae with females possessing stylets and males lacking them (Poinar, 1977). This assignment is congruous with cases of extant nematode parasitism of phorids, consisting of a single described species of Howardula parasitizing the mushroom phorid, Megaselia halterata Wood (Richardson, Hesling & Riding, 1977; Poinar, 1975). Disney (1994) reported 4 additional species of Megaselia and 2 species of Woodiphora as hosts of nematodes, presumably Howardula; however, none of these have been studied in detail.

Systematics

Tylenchida Filipjev

Allantonematidae (Pereira)

Howardula helenoschini n. sp. (Fig. 1)

Fig. 1. Howardula helenoschini n. sp. and phorid fly in Baltic amber. (A) Fly and 5 allantonematid nematodes. Insert shows different view of nematodes. Arrow shows specimen A [male ]; fleche shows specimen B [female]. (B) Head of specimen B. Arrow shows partial stylet in enclosing cast cuticle. (C) Head of specimen A. Magnification factor same as in (B). (D) Tail of specimen A. Arrow shows cloacal opening; fleche shows spicule. Magnification factor same as in (B).

Quantitative measurements are presented in Table 1, along with the corresponding measurements of H. husseyi from M. halterata, considered the closest extant member to the fossil. Both specimens A and B are partially coiled but lie on a single plane. Both nematodes appear to have been in the process of moulting or just finished moulting since 1 enclosing cuticle surrounds the anterior portion of specimen A and 2 enclosing cuticles surround the head of specimen B. The anterior ends of both nematodes are bluntly rounded to truncate while the posterior ends are narrowly pointed. The lip regions are not offset. The pharyngeal glands, excretory pore, nerve ring, lateral fields, bursa and gubernaculum could not be seen due to the state of preservation of the specimens. The vulva in specimen B was situated on a small protuberance and while uterine tissue was visible, the uterus proper was difficult to delineate. The cloacal opening in specimen A was also partly protruded and a structure inside the cloaca was interpreted to represent a spicule. The stylet in specimen B is visible only in the shed cuticle, thus only the anterior portion is present. The lemon-shaped female in the abdomen of the fossil phorid was 0·650 mm in length (the gravid females of H. husseyi range from 0·529–1·109 mm (Richardson et al. 1977)).

Type specimen: Deposited in the Poinar amber collection.

Host: A female of the genus Triphleba (Diptera: Phoridae).

Etymology: Named after Mrs Helen Oschin.

DISCUSSION

Data on the extant H. husseyi and other species of Howardula parasitizing flies were used to interpret characters observed on the fossils. The gravid females of H. husseyi in the body cavity of the adult fly can be lemon-shaped, similar to that observed in the fossil fly. The males of H. husseyi moult 3 times successively and remain enclosed in their 3 cuticles while the females moult twice and remain surrounded by their cuticles. The retention of cast cuticles around the nematode is an indication of rapid development outside the host and also appears to be the case with H. helenoschini sp. n. In H. husseyi, the 2nd-stage nematodes leave the fly host via the intestine or reproductive system, usually when the host attempts oviposition in the mushroom compost (Richardson et al. 1977). However, in H. neocosmisPoinar, Jaenike & Shoemaker (1998) parasitizing Drosophila flies, the 3rd-stage juveniles leave the host and moult twice in the environment to the adult stage. In both the above species, fertilized females boring through the body wall of the larval host initiate infection.

While gravid females of H. husseyi are capable of producing between 300 and 850 eggs, in the present case, only 5 progeny were present. Additional nematodes may still remain inside the fossil fly (none could be seen, however) and other juveniles may have already been released from the fly on previous oviposition attempts. Even if one or both of these scenarios is correct, it appears that the number of progeny of H. helenoschini is fewer than those of H. husseyi and other Howardula species (Richardson et al. 1977).

While the small number of progeny could be related to the small host size (only 1·2 mm in length), it could represent an early stage in the development of parasitism in this nematode clade. Another difference is the large size of the juveniles (larger than any of the other described members of the genus Howardula, which range from 250 to 600 μm in length (Richardson et al. 1977; Poinar et al. 1998). During the development of parasitism in many nematode lines, there is an increase in size of the gravid female with an increase in progeny number and a smaller body size of individual progeny (Poinar, 1983). Thus, the small number of progeny coupled with the larger size of the juveniles could indicate an early stage in the adaptation of these nematodes to their host.

Another possible explanation for the small number of progeny is that the parasites may have not yet completely adapted physiologically to their host, especially regarding the fly's immune system. The gravid females of H. husseyi are often surrounded by host haemocytes (Riding & Hague, 1974). It is likely that these haemocytes are responding to the presence of the parasite and attempting to wall it off. At an earlier evolutionary stage, such a reaction would be expected to be more severe and could seal off or kill the female before all her progeny are released.

Members of the phorid genus Triphleba are necrophagous (Stone et al. 1983) and at least 2 species have been described from Baltic amber (Evenhuis, 1994). The present fossil fly is very similar to T. praeterita Brues, which is relatively common in Baltic amber, with adults ranging from 1·2 to 1·4 mm in length (Brues, 1939).

In the present case, it is likely that the parasitized female Triphleba inadvertently landed in a resin deposit on the amber-producing tree. The 5 nematode specimens exited from the host, either via the anus or genital tract, as they do in the case of H. husseyi (Richardson et al. 1977) and other species of Howardula attacking drosophilids (Poinar et al. 1998). The moults suggest that the nematodes survived for some hours on the surface of the resin, obtaining enough oxygen to mature to the adult or pre-adult stages before being covered by a subsequent resin flow.

The author thanks Michael Oschin for allowing him to describe this interesting nematode species from his collection and for donating the specimen to the Poinar amber collection, Brian Brown for identifying the genus of Phoridae and Roberta Poinar for editorial comments.

References

REFERENCES

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Figure 0

Fig. 1. Howardula helenoschini n. sp. and phorid fly in Baltic amber. (A) Fly and 5 allantonematid nematodes. Insert shows different view of nematodes. Arrow shows specimen A [male ]; fleche shows specimen B [female]. (B) Head of specimen B. Arrow shows partial stylet in enclosing cast cuticle. (C) Head of specimen A. Magnification factor same as in (B). (D) Tail of specimen A. Arrow shows cloacal opening; fleche shows spicule. Magnification factor same as in (B).

Figure 1

Table 1. Measurements (in μm) of Howardula helenoschini n. sp. (specimen A-[male ] and specimen B-[female]) and H. husseyi free-living stages (after Richardson et al. 1977)