PHEROMONE COMMUNICATION IN FEATHER-FEEDING WING LICE (INSECTA: PHTHIRAPTERA).

Pheromone communication is central to the life history of insect parasites. Determining how pheromones affect parasite behavior can provide insights into host-parasite interactions and suggest novel avenues for parasite control. Lice infest thousands of bird and mammal species and feed on the host's feathers or blood. Despite the pervasiveness of lice in wild populations and the costs they exact on livestock and poultry industries, little is known about pheromone communication in this diverse group. Here, we test for pheromone communication in the wing lice (Columbicola columbae) of Rock Doves (Columba livia). Wing lice spend the majority of their lives on bird flight feathers where they hide from host preening by inserting their bodies between coarse feather barbs. To feed, wing lice must migrate to bird body regions where they consume the insulating barbs of contour feathers. We first show that wing lice readily form aggregations on flight feathers. Next, using a Y-tube olfactometer, we demonstrate that wing lice use pheromone communication to move toward groups of nearby conspecifics. This pheromone is likely an aggregation pheromone, as wing lice only produce the pheromone when placed on flight feathers. Finally, we found that when forced to choose between groups of male and female lice, male lice move toward male groups and females toward female groups, suggesting the use of multiple pheromones. Ongoing work aims to determine the chemical identity and function of these pheromones.

Evidence for idiothetic and allothetic control of thermo-orientation in feather-feeding lice.

Thermal cues are widely used by ectoparasites to find and exploit hosts. Recently, the wing louse Columbicola columbae (Phthiraptera: Ischnocera) was shown to use thermo-orientation when migrating between host microhabitats. Here, we study the control systems governing thermo-orientation by motion tracking wing lice on spatial and temporal heat gradients. As previously demonstrated, lice placed on spatial heat gradients successfully located nearby heat targets. Unilateral antennectomies were then used to remove spatial aspects of the thermal cue. These lice were still capable of locating heat targets, suggesting their response relied on tracking changes in the cue over time (idiothetic control). Course control was accomplished via angular corrections after louse body-angles deviated from the heat target. Louse behavior on temporal heat gradients provided additional evidence for idiothetic control- lice altered turn size and velocity after temperatures uniformly shifted without any spatial reference. We also show that lice are likely capable of responding to spatial aspects of the cue, consistent with allothetic control. On the spatial heat gradient, lice with two antennae were more efficient at locating heat targets as compared to those with unilateral antennectomies. Additionally, when traveling along temperature isoclines (where lice can detect spatial but not temporal aspects of the cue), lice with two antennae consistently turned towards the heat target, while those with unilateral antennectomies showed no preference. In all, we find evidence that lice can use both idiothetic and allothetic control during thermo-orientation, and likely integrate information from these two systems to guide movements on hosts.

Thermo-orientation and the movement of feather-feeding lice on hosts.

Temperature variation on the host is known to influence ectoparasite distributions. Ectoparasites may also use temperature gradients between host regions when moving on the host; however, tests are rare. Feather-feeding wing lice (Phthiraptera: Ischnocera) spend the majority of their time on the flight feathers of their avian hosts where they insert their bodies between feather barbs to escape host preening. However, because wing lice feed on downy abdominal feathers, they must repeatedly migrate between the flight feathers and body regions of their hosts. We performed a series of experiments that tested thermo-orientation in wing lice and evaluated its potential use during louse migrations between host regions. We found that wing lice can rapidly and accurately locate nearby heat targets that approximate host temperatures (37 C), demonstrating a capacity for directed thermo-orientation. We next tested the preference of wing lice for temperatures found along migration routes between bird flight feathers and their body regions. Wing lice could distinguish between temperatures found within distinct bird regions, and lice that had recently fed preferred the cooler temperatures (32 C), similar to those within bird flight feathers where they typically reside. However, when starved for 18-20 hr, wing lice shifted their preferences toward temperatures typical of bird body regions where they feed (36 C), demonstrating an ability to use thermal cues when moving between bird regions. We discuss the use of thermal cues during louse migration and microhabitat selection, as well as other potential impacts of thermo-orientation on host-parasite interactions.

Community interactions govern host-switching with implications for host-parasite coevolutionary history.

Reciprocal selective effects between coevolving species are often influenced by interactions with the broader ecological community. Community-level interactions may also influence macroevolutionary patterns of coevolution, such as cospeciation, but this hypothesis has received little attention. We studied two groups of ecologically similar feather lice (Phthiraptera: Ischnocera) that differ in their patterns of association with a single group of hosts. The two groups, "body lice" and "wing lice," are both parasites of pigeons and doves (Columbiformes). Body lice are more host-specific and show greater population genetic structure than wing lice. The macroevolutionary history of body lice also parallels that of their columbiform hosts more closely than does the evolutionary history of wing lice. The closer association of body lice with hosts, compared with wing lice, can be explained if body lice are less capable of switching hosts than wing lice. Wing lice sometimes disperse phoretically on parasitic flies (Diptera: Hippoboscidae), but body lice seldom engage in this behavior. We tested the hypothesis that wing lice switch host species more often than body lice, and that the difference is governed by phoresis. Our results show that, where flies are present, wing lice switch to novel host species in sufficient numbers to establish viable populations on the new host. Body lice do not switch hosts, even where flies are present. Thus, differences in the coevolutionary history of wing and body lice can be explained by differences in host-switching, mediated by a member of the broader parasite community.

Geographic variation in the community structure of lice on western scrub-jays.

Parasites are incredibly diverse. An important factor in the evolution of this diversity is the fact that many parasite species are restricted to 1, or just a few, host species. In addition, some parasites exhibit geographic specificity that is nested within their specificity to a particular species of host. The environmental factors that restrict parasites to particular regions within the host's range are poorly understood, and it is often difficult to know whether such patterns of geographic specificity are real, or merely artifacts of uneven host sampling. For over a decade, we sampled communities of ectoparasitic lice (Phthiraptera) from western scrub-jays (Aphelocoma californica) throughout their range in the United States, and found 3 common species of lice. Philopterus crassipes was found throughout the host range, whereas the other 2 species of lice had more restricted distributions. Brueelia deficiens was found only on the woodhouseii host subspecies group, and Myrsidea sp. was found largely on the californica host subspecies group. We suggest that differential tolerance to arid conditions and interspecific competition has led to the restricted geographic distributions of these 2 species of lice.

A hitchhiker's guide to parasite transmission: The phoretic behaviour of feather lice.

Transmission to new hosts is a fundamental challenge for parasites. Some species meet this challenge by hitchhiking on other, more mobile parasite species, a behaviour known as phoresis. For example, feather-feeding lice that parasitise birds disperse to new hosts by hitchhiking on parasitic louse flies, which fly between individual birds. Oddly, however, some species of feather lice do not engage in phoresis. For example, although Rock Pigeon (Columba livia) "wing" lice (Columbicola columbae) frequently move to new hosts phoretically on louse flies (Pseudolynchia canariensis), Rock Pigeon "body" lice (Campanulotes compar) do not. This difference in phoretic behaviour is puzzling because the two species of lice have very similar life cycles and are equally dependent on transmission to new hosts. We conducted a series of experiments designed to compare the orientation, locomotion and attachment capabilities of these two species of lice, in relation to louse flies. We show that wing lice use fly activity as a cue in orientation and locomotion, whereas body lice do not. We also show that wing lice are more capable of remaining attached to active flies that are walking, grooming or flying. The superior phoretic ability of wing lice may be related to morphological adaptations for life on wing feathers, compared to body feathers.

COMPARATIVE TRANSMISSION DYNAMICS OF COMPETING PARASITE SPECIES.

Competition-colonization trade-off models explain the coexistence of competing species in terms of a trade-off between competitive ability and the ability to colonize competitor-free patches of habitat. A simple prediction of these models is that inferior competitors will be superior dispersers. This prediction has seldom been tested in natural populations because measuring dispersal is difficult. Host-parasite systems are promising in this regard, especially those involving "permanent" parasites that complete their entire life cycle on the body of the host. Because of this close association with the host, the dispersal, i.e., transmission, of these parasites can be monitored very accurately. We tested the dispersal prediction of the competition-colonization model by documenting the transmission dynamics of feather-feeding lice, which are permanent, relatively host-specific parasites of birds. We compared two groups known as "wing" lice and "body" lice that are common parasites of Rock Pigeons (Columba livia Gmelin). The two groups are ecologically similar, and they compete for resources on the host. Previous work shows that body lice are competitively superior to wing lice, leading us to predict that wing lice should be better than body lice at dispersing to new host individuals. We tested this prediction by comparing the ability of wing and body lice to disperse between hosts using vertical- and horizontal-transmission mechanisms, including phoretic hitchhiking on parasitic flies (Diptera: Hippoboscidae). A series of experiments with both captive and wild birds confirmed that wing lice are much better than body lice at colonizing new hosts. Wing lice showed significantly greater vertical transmission to nestlings, and they were quite capable of phoretic transmission to new hosts on flies. In contrast, body lice were not phoretic. These results provide the first rigorous demonstration of phoretic transmission in lice, and they underscore the importance of a community-level approach to understanding the ecology of parasite transmission dynamics.