Sometimes the fossil record just gives us a gift, something that moves our understanding to an all-new level. One such gift saw publication a couple of years ago, but unfortunately I didn’t have time to write about it then. I think it’s about time I corrected that lacuna.
By this point in time, we have a pretty good understanding of the basal framework of harvestmen evolution. The mite-like harvestmen of the Cyphophthalmi are well established as the sister group to all other Opiliones (which form a clade called the Phalangida). Unique features of the Phalangida include an intromittent penis in the males (phalangids are one of the few groups of arachnids to possess such a feature) and a central eyemound with a single pair of eyes. The Cyphophthalmi are more heavily armoured than most phalangids, and have a characteristic pair of raised cones (the ozophores) on either side of the carapace near the front that support the openings of odour-producing repugnatorial glands. Until recently, it was thought that most Cyphophthalmi lack eyes, but tiny, lens-less remnant eyes are now known to be present at the base of the ozophores in many cyphophthalmid subgroups.
There had long been questions about the nature of the cyphophthalmid eyes. The original arachnids possessed multiple pairs of eyes, and there is a good case to be made that the basal arrangement for arachnids as a whole is a single pair of larger median eyes in the middle of the carapace, and a number of pairs (up to three) of smaller lateral eyes at the margin. In some arachnid groups the median eyes have been lost; in others, the lateral eyes have become reduced in number or lost. In spiders, the lateral eyes have become enlarged and shifted about so the lateral/median distinction is less applicable (for the record, the posterior median eyes in spiders correspond to the original median eyes). Mites, of course, being mites, mess the whole system up entirely. Most mite eyes correspond to the original lateral eyes, but some mites possess a single median eye whose relation to the original arachnid median eye pair is up for grabs.
Phalangids, with their single central eyemound and single pair of eyes, had obviously kept the original median eyes and lost the lateral eyes. But what had happened with the Cyphophthalmi? Did their single pair of eyes near the edge of the carapace represent a single remnant pair of lateral eyes, or did they correspond to the median eyes of other Opiliones? It should be noted that some derived groups of undoubted Phalangida have lost the eyemound and have their eyes sitting directly on the carapace, and in some cases these unraised eyes may be widely separated. Arguments for both interpretations of cyphophthalmid eyes had been put forward by different authors, but the matter had certainly not been decided.
That was until the description by Garwood et al. (2014) of Hastocularis argus, a remarkably preserved fossl harvestman from the Carboniferous of France. The appearance of this animal was established in some detail by the use of microtomography, allowing a number of details about it to be established. It was a heavily armoured animal with long legs, and like modern Phalangida it possessed a central eyemound on which there had been a pair of eyes (the eyes themselves were not preserved, but the sockets that had originally contained them were). The use of microtomography also allowed the identification of an intromittent penis like a phalangid. But Hastocularis also possessed a pair of raised ozophores like modern Cyphophthalmi, and at the base of those was preserved another socket indicating the presence of a second pair of eyes. There really could not be a more perfect answer to the cyphophthalmid eye question: the immediate ancestor of the Opiliones possessed two pairs of eyes, and the eyes of Cyphophthalmi do indeed correspond to the lateral eyes of other non-harvestmen arachnids and not to the median eyes of phalangids*.
*Pedantically speaking, Hastocularis is not the first four-eyed taxon assigned to the Opiliones. In 1875, an Austrian biologist by the name of Stecker described a remarkable animal from the Sudeten Mountains of Bohemia under the name of Gibbocellum sudeticum. Gibbocellum bore an overall resemblance to the Cyphophthalmi, except for possessing two pairs of eyes on raised cones, as well as two pairs of spiracles (other Opiliones possess a single pair). Despite enthusiastic searches, no other naturalist was ever able to find further specimens of Stecker’s species, and at least one author suggested that it might be a poorly interpreted pseudoscorpion. However, a close criticism of various irregularities in Stecker’s publications on Gibbocellum eventually lead Hansen & Sørensen (1904) to the conclusion that it had not merely been misrepresented, but was in fact a complete fabrication on that author’s part.
A phylogenetic analysis of Hastocularis lead Garwood et al. (2014) to believe that it was more closely related to Cyphophthalmi than to Phalangida; together with another Carboniferous fossil species, Eophalangium sheari, they placed it within a new taxon Tetrophthalmi (meaning, of course, ‘four eyes’). The main features cited in support of this relationship were the complete fusion of the dorsal surface (the only other harvestmen to show this feature are a southeast Asian family, the Oncopodidae, who are too deeply nested within the Phalangida to be a likely direct relative of Hastocularis) and the genital opening being a broadly open gonostome (in Phalangida, the genital opening is covered by an operculum). This implies that the immediate ancestor of all Opiliones was relatively long-legged, with the short legs of Cyphophthalmi a derived feature. However, I personally find the presence of an intromittent penis in Tetrophthalmi (it is also known to be present in Eophalangium) somewhat problematic in this regard. As noted above, the phalangid intromittent penis that directly injects sperm into the female ovipositor is highly unusual among arachnids. Cyphophthalmi do possess a penis-like structure (called the spermatopositor) but it is much shorter than in any phalangid and does not function as an intromittent organ. Instead, Cyphophthalmi males produce an encapsulated spermatophore that is attached by the spermatopositor to the female’s underside, a more typical sort of arrangement for arachnids as a whole. An intromittent penis in the cyphophthalmid stem group would imply that Cyphophthalmi somehow reverted towards a more primitive-seeming reproductive arrangement at some point in the past. One possibility is that the penis of Tetrophthalmi did not function in exactly the same manner as that of Phalangida: perhaps tetrophthalmids still produced a spermatophore but were able to insert it more deeply in the female than Cyphophthalmi? Another possibility may be that Tetrophthalmi are stem-phalangids rather than stem-cyphophthalmids; only further analyses can possibly tell us more.
Garwood, R. J., P. P. Sharma, J. A. Dunlop & G. Giribet. 2014. A Paleozoic stem group to mite harvestmen revealed through integration of phylogenetics and development. Current Biology 24: 1017–1023.
Hansen, H. J., & W. Sørensen. 1904. On Two Orders of Arachnida: Opiliones, especially the suborder Cyphophthalmi, and Ricinulei, namely the family Cryptostemmatoidae. University Press: Cambridge.