Recent phylogenetic analysis of mites in the superfamily Eriophyoidea, such as Aceria anthocoptes, suggest they originated from within the family Nematalycidae rather than as sister to Nematalycidae. (Photo credit: Gary Bauchan, Beltsville Agricultural Research Center, USDA)

By Samuel Bolton

Eriophyoidea, the superfamily of arthropods commonly known as gall mites (though not all of them form galls) or four-legged mites (though not all mites with four legs are in Eriophyoidea), are worm-like mites that are important and sometimes devastating parasites of plants. These mites represent one of the largest and earliest adaptive radiations of plant-parasitic arthropods; Triassic fossils show that this radiation was already well underway by 230 million years ago.

Samuel Bolton

Such an early transition to plant feeding has given this group ample time to diversify. Conservative estimates place this lineage at 100,000 living species, although to date only 5,000 species have been described. However, the true number could be considerably higher because almost all Eriophyoidea specialize on a species or genus of plant, and almost all vascular plants are host to one or more species of Eriophyoidea. Given that there are estimated to be around 300,000 species of vascular plants, a similar number of species of Eriophyoidea seems reasonable.

Arthropods in the family Nematalycidae (such as the Osperalycus tenerphagus protonymph, top) and superfamily Eriophyoidea (such as Aceria anthocoptes, bottom) both have elongated bodies lined with annular ridges. (Photo credit: Gary Bauchan, Beltsville Agricultural Research Center, USDA)

You might expect that the phylogenetic position of such a large lineage of mites would be known, but this is not the case. It’s still early days in the history of mite classification. Whereas many arthropod groups have their basal phylogenies more or less figured out, phylogenetic research on mites has been sorely neglected due to their small size. And because Eriophyoidea are among the smallest bodied mites (some are less than 0.1 mm in body length), it is perhaps not surprising that the taxonomic placement of this group is still unclear.

There has been a tendency to place all the major plant-parasitic lineages of mites into the large lineage of the order Trombidiformes. But the results of a recently published molecular phylogenetic analysis suggest that Eriophyoidea fall outside of Trombidiformes, although the lack of sampling of basal taxa does not show exactly where they belong.

Then where, exactly, do Eriophyoidea belong? One of the strongest candidates for a closely related taxon must be the Nematalycidae, a small family of deep soil mites. Indeed, it hardly takes an expert to spot similarities between Eriophyoidea and Nematalycidae: Both have worm-like bodies lined with annular ridges. In the past, some acarologists independently speculated on the possibility that these two taxa might be closely related, but this idea was not investigated further, perhaps because it did not seem likely that a group of plant parasitic mites could be closely related to a group of mites that live in deep soil. However, these two taxa share many characteristics other than just body shape, including a reduced number of limb segments and loss of certain body setae.

Although my collaborators Hans Klompen (Ohio State University, USA) and Philipp Chetverikov (Saint-Petersburg State University, Russia) and I predicted a close relationship between Eriophyoidea and Nematalycidae, our phylogenetic analysis of morphological characters, recently published in the journal Systematic and Applied Acarology, led to an unexpected result: Eriophyoidea originated from within Nematalycidae rather than as sister to Nematalycidae. However, because support for this relationship is not strong enough to rule out a sister relationship, more data is needed before we can confidently assert that eriophyoids are nematalycids.

One interesting implication of this discovery is that Eriophyoidea were probably somewhat preadapted for their parasitic lifestyle if they were descended from Nematalycidae. A narrow, elongate body, which provides an effective way of moving around the tight interstitial spaces of deep soil, would also appear to be useful for living in the constricted spaces on and inside plants. Although most of the Eriophyoidea that are around today are ectoparasites, they may have begun as an endoparasitic lineage that lived underneath the epidermis.

But this still leaves an interesting mystery: How did their ancestors shift from microbivory in deep soils to plant endoparasitism? Other than the requirement to move around in tight spaces, these two lifestyles could hardly seem more different.

Samuel Bolton, Ph.D., is Curator of Acari at the Florida State Collection of Arthropods, in the Florida Department of Agriculture and Consumer Services’ Division of Plant Industry. Email: samuel.bolton@freshfromflorida.com