The evolution and host‐relationships of the sucking lice of the Ferungulata
Authors: WEBB J. E. 
Published: August 2010

Summary.

An account is given of the structure of the spiracles of the majority of the species of the genera Linognathus, Solenopotes, Ratemia, Haematopinus, Microthoracius and Pecaroecus, including the nymphal spiracles of Linognathus pedalis and Pecaroecus javalii. A list of the species is given on page 134.
The host‐relationships of the genera Linognathus and Solenopotes are discussed. The spiracles of lice of these two genera form a more or less continuous series and are therefore treated together. This series can be divided into three main groups the largest of which, with the spiracles of L. pedalis as a more or less central type, comprises species from members of the Alcelaphini of the Hippotraginae, the Antilopinae, the Cephalophinae, the Caprinae, the Bovinae, the Giraffidae and the Cervidae. The spiracles in this group form a continuous series of modifications. The second group comprises two species, L. fahrenholzi and L. hippotragi from members of the Hippotragini and Reduncini of the Hippotraginae. The third group includes L. setosus and probably L. taeniotrichus from Canidae and also L. ovillus from the domestic sheep. This last group is almost certainly unnatural, the similarity in the spiracles of L. setosus and L. ovillus in all probability being due to convergence and not indicative of close affinity.
It is concluded from a study of their sucking lice that the Caprinae, Bovinae and Cephalophinae form a more or less closely related central group of the Bovidae with the Antilopinae and the Alcelaphini of the Hippotraginae respectively, of rather more distant origin and more closely related, one to another, than either is to the Caprinae.
The spiracles of Linognathus gnu and L. damaliscus from members of the Alcelaphini of the Hippotraginae are near those of lice infesting members of the Antilopinae. The spiracles of L. fahrenholzi and L. hippotragi from members of the Reduncini and Hippotragini, also of the Hippotraginae, on the other hand, are as widely different from those of L. gnu and L. damaliscus as this rather compact group allows. Thus, according to the evidence derived from louse affinities, it would appear that the Hippotraginae is probably an unnatural assemblage, since the lice from Alcelaphini show affinities with those from the Antilopinae, while lice from the Hippotragini and Reduncini fall together as a group, showing no close affinity either with those from the Alcelaphini or, for that matter, with any Siphunculata here examined from any Bovidae. Simpson (1945), who has defined the Hippotraginae, has expressed doubts as to its validity.
The position of lice of the genus Solenopotes from Cervidae, near those from members of the Bovinae, suggests some relationship between the Cervidae, on the one hand, and a central group of the Bovidae on the other. Furthermore, the intermediate position of Linognathus brevicornis from the giraffe between cervid and bovid lice upholds the view that the Giraffidae arose, either as an early offshoot from the Cervidae, or from a position somewhere between the Bovidae and Cervidae at a time shortly after this bifurcation took place.
The possibility of Canidae acquiring lice from sheep or vice versa to account for the similarity in spiracle structure in Linognathus setosus and L. ovillus is discussed. The view adopted is that, in all probability, L. setosus is normal to Canidae, or at least was acquired at a very early date, possibly long before the sheep had been evolved, and that L. ovillus is normal to the sheep, the similarity of spiracles in L. setosus and L. ovillus being fortuitous.
The host‐relationships of the genus Ratemia are discussed. R. squamulata is claimed to possess undeniable affinities with the genus Linognathus because of its spiracle structure, but, at the same time, presents characters more in keeping with Microthoracius, Pecaroecus and Haematopinus. Ratemia is known only from Perissodactyla and, as it may be considered a relative of Linognathus, then the existence of lice of the linognathoid type on the Artiodactyla, Carnivora and Perissodactyla suggests a probable common origin for these three eutherian orders.
The host‐relationships of the genus Haematopinus are discussed. With the exception of the spiracles of H. taurotragi, the degree of variation between spiracles of different species is very small. The species fall into three groups: firstly, those in which the spiracles are small relative to body length and bear traces of a ledge system on the atrial walls–these species infest Equidae; secondly, those in which the spiracles are large relative to body length and also retain traces of a ledge system–these species infest Bovidae; thirdly, those in which the spiracles are small relative to body length, but retain no traces of ledges even in the nymph–these species infest Suidae. The fact that the species of Haematopinus fall into three groups coincident with the grouping of the hosts, suggests that none of these infestations is of particularly recent date and that Haematopinus was either present on a common ancestor of the Equidae, Bovidae and Suidae or else, if straggling did take place, that the parasites were acquired comparatively early in the evolution of their hosts. The possible causes of the discontinuous distribution of Haematopinus are discussed, and it is thought more probable that lice of this genus are normal to their hosts and were present on the common ancestor of the Artiodactyla and Perissodactyla than that they achieved their present distribution by extensive straggling, though some degree of straggling is not excluded as a possible contributory cause.
The difference in spiracle structure between Haematopinus taurotragi and other species of that genus infesting Bovinae is greater than might be expected, in view of the comparatively close relationship between their hosts. This distinction, however, may reflect their host affinities, for H. taurotragi infests a member of the tribe Strepsicerotini, whereas other species with which it is here grouped are from members of the tribe Bovini of the same subfamily, the Bovinae. It should be noted, however, that the differences in spiracle structure involved are greater than those between all other species of Haematopinus, even though their hosts are far more widely separated, as in the case of species from Equidae and Suina.
The host‐relationships of the genus Microthoracius are discussed. It is noted that the spiracles of species from the Old and New World Camelidae show a close similarity indicating a high degree of stability in this structure, in view of the fact that the hosts must have been separated since the Pliocene period and possibly earlier. Species of Microthoracius from llamas possess spiracles which are closer to one another than they are to those of species from the camel. It is considered that the spiracles in Microthoracius are nearer to those of Linognathus than to those of Haematopinus, though probably not derived directly from either. The close association of Microthoracius with other genera of lice infesting Ferungulata, in spite of its specialized body form, is in keeping with the phylogeny of the hosts, although it casts no fresh light on the origin of the Tylopoda.
The host‐relationships of the genus Pecaroecus are discussed. P. javalii, from the collared peccary, is a louse possessing more generalized characters than any other from Ferungulata and yet has spiracles almost identical with those of Haematopinus, and as specialized as any found within the group. The affinities of this louse lie rather with Haematopinus than with Linognathus, although, like Microthoracius, it is clearly not derived directly from either. The affinities of the Tayassuidae are not particularly clarified by the relationships of Pecaroecus.
An analysis of the main characters of each genus of sucking lice infesting members of the Ferungulata is made. It is evident from this study that the twelve genera considered fall broadly into two groups, the first called the linognathoid group comprises the genera Linognathus, Solenopotes, Ratemia, Microthoracius and Prolinognathus; the second, the haematopinoid group, comprises the genera Haematopinus, Pecaroecus, Hybophthirus, Echinophthirius, Proechinophthirus, Antarctophthirus and Lepidophthirus.
On a basis of comparison of 16 generic characters, it is concluded that Pecaroecus is the most generalized genus of sucking louse from Ferungulata and that Haematopinus is only slightly less primitive. It is held to be improbable that Haematopinus was derived directly from Pecaroecus, although the two genera evidently originated from the same stock.
The genus Hybophthirus from Tubulidentata, although more specialized, has a number of characters in common with Haematopinus and could be a direct derivative from that form.
The pinnipede‐infesting genera, Echinophthirius, Proechinophthirus, Antarctophthirus and Lepidophthirus are evidently derived from a common ancestral genus, and therefore are considered together. In spite of their extreme specialization, sufficient remains of their fundamental body plan to indicate that they have either arisen from Haematopinus or from a form very near that genus.
Among the genera included in the linognathoid group the greatest number of primitive characters are to be found in Linognathus, although this form is not nearly so generalized as Pecaroecus or Haemtopinus. It is concluded that, although Linognathus and Haematopinus are related, neither could have been derived directly from the other, nor could Pecaroecus itself have been ancestral to Linognathus. It is thought probable that both Linognathus, on the one hand, and Pecaroecus and Haematopinus, on the other, represent two branches of a bifurcation arising from a still more primitive ancestral form.
The genus Prolinognathus is related to Linognathus and, although more specialized in some respects, it retains some important primitive features not found in the latter. Here, again, neither Linognathus nor Prolinognathus could have been ancestral to one another as such. The most probable interpretation of the facts is that Prolinognathus is an early offshoot from a stock later giving rise to Linognathus.
Another genus related to Linognathus is Ratemia. Ratemia is, however, more primitive than Linognathus in some respects, and more specialized in others. Ratemia, too, could not have been derived directly from Linognathus, although it may well have arisen from the same stock, possibly at a later date or at about the same time as Prolinognathus.
A genus less surely to be assigned to the linognathoid group is Microthoracius. In spite of its possession of a number of primitive characters in common with Pecaroecus, in the form of the spiracles and in other respects it is definitely linognathoid in character. It is tentatively concluded, therefore, that Microthoracius is an early offshoot from somewhere near the base of the linognathoid stock, possibly a little later than Prolinognathus in view of the structure of its spiracles.
The genus Solenpotes appears to be almost certainly a direct derivative of Linognathus.
It is suggested that some of the characters used in the classification of the Siphunculata have arisen independently, on a number of separate occasions and therefore are not necessarily indicative of particularly close affinity. An example cited here is the parallel development of atrial sculpture in the spiracles of Siphunculata and Trichodectidae from simple beginnings in a manner which is thought to be non‐adaptive. The close resemblance of spiracles from Trichodectes canis and Linognathus vituli is such as might be expected from species of the same genus, rather than from members of two distinct suborders.
It is considered that the most efficient type of spiracle serving as a dust trap in the Siphunculata is one in which processes project into the atrium from the atrial wall. The most primitive spiracles in that suborder are very small and have the beginnings of such an arrangement in the minute spines which cover the internal atrial wall. This sculpturing, however, is not elaborated as the spiracle increases in size, the minute spines being replaced as the functional mechanism for retaining dust within the atrium by a less efficient system of annular and cross‐ledges. It is only in the most advanced spiracles that the ledge system is broken down, leaving the points of junction of the ledges projecting into the atrium as atrial processes of one type or another. The same indirect method of forming atrial processes is adopted in both Siphunculata and Trichodectidae. There is evidence, too, to suggest that such atrial processes have been formed independently, in the same manner, in a number of genera and species within the Siphunculata themselves.
It is noted that cross‐ledges joining annular ledges are not formed in spiracles of diameter less than about 20 μ. In spiracles above 20 μ diameter cross‐ledges appear to be formed almost invariably, and in a series of species of Linognathus, in which both annular and cross‐ledges are characteristically present in the spiracles, a presumed secondary reduction in spiracle size results in the almost complete disappearance of cross‐ledges at about an atrial diameter of 20 μ. Furthermore, in a related series of species of Linognathus, the number of crossledges present on the atrial wall increases approximately directly as the atrial diameter increases above 20 μ. Not all species of Linognathus, however, fall within this series, as in some the ratio between number of cross‐ledges and atrial diameter is significantly different. The appearance or disappearance of cross‐ledges in a spiracle of diameter greater or less than 20 μ is evidently not due to the mechanical impossibility of forming cross‐ledges at less than a certain distance apart, for the spatial arrangement of ledges in the spiracle of the first nymph of Linognathus pedalis is so close that there is ample room in a spiracle of less than 20 μ diameter, to develop some cross‐ledges equally closely spaced. The lower limit of 20 μ atrial diameter for the development of cross‐ledges appears to apply equally to spiracles of both Siphunculata and Trichodectidae.
It is suggested that, in sucking lice from Ferungulata, a number of characters other than atrial sculpture have been developed independently by different genera. Among these are included the reduction of the anterior pair of legs and enlargement of the posterior pairs, the fusion of tibia and tarsus, the reduction of eyes and the partial or complete reduction of some or all of the selerotic plates of the thorax and the abdomen. It is stressed that, in view of widespread parallel evolution, great care is needed in analysing the complex mixture of generalized and specialized characters to be found in all forms of lice existing to‐day, before an assessment of their affinities is attempted.
It is stressed that the validity of any assumptions of eutherian affinities based on those of their louse fauna is subject to the provision that any particular louse is normal to its host, that is, the infestation is of a primary and not a secondary nature due to straggling, however ancient, from a host of one species to one of another, even of the same genus. A permissible exception to this rule occurs when host affinities are inferred from parasites which, although they may have originated on the ancestral host stock by straggling, have infested the same line of hosts for the entire period during which the evolutionary developments of the hosts took place.
It is suggested that transference of lice takes place either from parent to offspring or between members of opposite sexes. The virtual absence of obligate ectoparasites in any group other than the birds and mammals, is attributed to the fact that only in the higher vertebrates is parental care sufficiently well developed to ensure comparatively certain transference of parasites.
The low incidence of straggling in view of the high degree of host specificity shown by Siphunculata is noted. It is thought possible, however, that the establishment of louse species on alien hosts might have been easier at a time early in the evolution of the Eutheria, when the various orders must have been nearer to one another physiologically than they are to‐day and host specificity on the part of the parasite less highly developed. Straggling occurring at such a time might now be difficult, if not impossible, to detect.
It is concluded that, as the Siphunculata from Ferungulata evidently form a natural group and as the Ferungulata, too, is presumably a natural group, the presence of these lice, as a whole, on the Ferungulata is the result of one or more primary infestations dating back to the inception of the host group. Similarly, as most of the groups within the Ferungulata harbour lice characteristic of themselves, these, too, are probably also derived from later primary infestations.
The existence of primary infestations of Haematopinus and Linognathus on Carnivora and Artiodactyla and of Haematopinus on Perissodactyla, suggest that lice of those genera infested the common ancestors of these eutherian orders. It is concluded, therefore, that the genera Linognathus and Haematopinus must have been in existence since, at the earliest, the end of the Cretaceous and possibly the beginning of the Palaeocene period and that, by that time, lice on the Ferungulata had run through the entire range of evolution of atrial sculpturing of their spiracles, later evolution involving only minor modifications of existing atrial types. Thus, phylogenies of parasite and host based on the main types of atrial sculpture, and other characters are referable to the period during which the great majority of the eutherian orders became differentiated.
It is thought that the ancestral stock of the Ferungulata must have been infested with at least three, and probably more, genera of sucking lice, namely, Haematopinus, Linognathus and the ancestor or ancestors of Pecaroecus, Microthoracius, Ratemia and Prolinognathus. The lice of Ferungulata as seen to‐day are probably the remnants of a much more extensive fauna which, like their hosts, reached a peak of diversification and have since largely become extinct through interspecific and intergeneric competition among the lice themselves and through the extinction of their hosts. Thus, through different genera of lice surviving on each host group and later undergoing speciation, the present position of a number of genera of lice, each characteristic of a single ferungulate group, would arise.
As the affinities between lice can only be of value in determinations of host relationships if the lice in question had been evolved on the host stock after that stock had become differentiated, it is evident that some louse affinities will bear little relationship to those of their hosts. Forms such as Pecaroecus and Microthoracius evidently date back to a time long before either of the host groups had become separated off from their ancestral stock, and their existence on peccaries and camels does not mean that those mammals are of exceptionally ancient origin. Thus, the use of louse affinities as a guide to eutherian phylogeny is limited to the following cases: firstly, the relationships between large groupings of lice where these occur on equally circumscribed groups of mammals, such as the probable relationship between ferungulate lice and those characteristic of many rodents as indicating a probable origin of the Ferungulata themselves from the base of the rodent stock; secondly, the indication of common origin of some eutherian orders, though not necessarily of close affinity, provided by the wide distribution of a genus and its derivatives, such as the distribution of Haematopinus, and derivatives on Artiodactyla, Perissodactyla, Carnivora and Tubulidentata; thirdly, the comparatively recent interspecific or occasionally intergeneric relationships, where the genera are close, of lice infesting definite restricted host groups, such as Linognathus and Solenopotes on Pecora and Haematopinus on Equidae.