We were able to successfully track patterns of louse movement in a population of wild M. rufus. Recorded transfers occurred exclusively between males which may have been due to male-male contact resulting from nest-hole sharing , agonistic interactions occurring during the breeding season , or from multiple males mating with the same female. No females, however, were ever found to have lice on or near the genitals. The transfers were quite evenly distributed throughout the study area and showed no consistent distance, direction or clustering patterns. This pattern of transfer contrasts with mouse lemur trapping data in the study area. Most of the louse transfers occurred between lemurs over 100 m from each other, and one transfer (between Rac and Nap, Figure 1a) spanned over 600 m. The transfers therefore demonstrate a degree of lemur ranging far greater than anticipated using standard trapping methods (Additional file 8: Table S3). They also provide evidence of a lemur social network that could not have been predicted based on trapping data alone (Additional file 3: Figure S3, Additional file 4: Figure S4, and Additional file 5: Table S1). Moreover, relatively few individual lemurs with broad ranging patterns appear to be largely responsible for the long-distance transfer of lice. These patterns of parasite-host dynamics suggest that a small number of individuals can quickly spread parasites throughout the population.
As hypothesized, transfers increased significantly at the beginning of the breeding season, indicating an increase in host interactions. We found that transfers occurred most frequently and nearly exclusively during the breeding season. This combined with the restriction of transfers to male hosts suggest that the transfers were due to agonistic same-sex interactions associated with the breeding season. A previous study  in chipmunks indicated that breeding periods correspond to an increase in rates of louse transfer, but there are also arguments that louse transfer in general is not a common occurrence [6, 16]. The 76 transfers we tracked between 14 animals over the course of four weeks are therefore remarkable both with respect to the high rate at which they occurred, and their correlation with the breeding season.
Although no marked lice were recaptured on female lemurs, it is possible that they were involved as intermediaries in male-male transfers. All transfers observed required at least one incidence of direct contact; however, it is possible that an intermediate host could have facilitated these transfers between what we record as the donating and receiving hosts. Thus it is possible that a female received a louse from one male during a copulation event and transferred it to second male during a later copulation. This is unlikely to be a common occurrence, however, as we only observed a single louse on a single female host over the entire duration of the study. Additionally, testosterone is known to increase the transmission potential of certain parasites , suggesting that the high testosterone levels seen in male mouse lemurs may increase the transmission potential of louse-borne pathogens. Testosterone has also been implicated as an immunosuppressant [18–22], and during the reproductive season animals experiencing increases in testosterone are more likely to be vulnerable to parasitic infestation [17, 23, 24]. An increase in testosterone levels as the males invest in spermatogenesis for the annual breeding season may be a mechanism underlying the all-male transfers.
Lice previously marked on the ears of one host were most frequently recaptured on the testes of that same host or other hosts, rather than the ears. The frequent migration of lice to the testes and the presence of all stages of the louse life cycle there indicate that this is a preferred attachment site, potentially because of the area's rich peripheral blood supply and relatively sparse fur leading up to and during the breeding period when they are dramatically distended (see Additional file 9: Figure S6 for an example). The timing of this increase in louse populations about one week before host breeding indicates that lice may be triggered to reproduce by increasing levels of host sex hormones in their bloodmeals as occurs in at least two species of fleas that parasitize rabbits . This could explain the appearance of lice on the testes immediately before the beginning of the breeding season. We found no correlation between louse intensity and testicular volume in the 14 males involved in transfers (Table 1, also see Additional file 10: Text S1 for more information).
The variation in donor scores indicates that host individuals do play varying roles in the transfer of lice and transmission of their potential pathogens throughout the population. Age of the host may be a factor determining which hosts act more as donors. Durden (1983)  observed that juvenile hosts did not act as donors in louse transfers despite having larger louse infestations than adults. Indeed, the youngest host in this study had the heaviest louse infestation but donated only one louse. However, we found no overall correlation between the age of the host and louse transfers (Table 1, also see Additional file 10: Text S1 for more information), and the divide between 'donors' and 'recipients' does not appear to be the result of testicular volume, age or body mass.
Vector potential scores, like donor scores, ranged widely between individuals; however, the two are not significantly correlated. Vector potential scores therefore provide a second distinct way of assessing the impact an individual lemur host can have on patterns of louse transmission and population-wide pathogen transmission. The evidence of multiple host transfers also suggests a heightened probability of potential pathogen transmission as the probability for lice contacting and carrying a blood-borne pathogen increases with exposure to blood from an increasing number of hosts. Of the four animals removed from the distance analysis (Figure 3) one individual (Mam) was responsible for transfers over both short and long centroid-based distances. Interestingly, this same male was revealed by the vector potential analysis (not influenced by distance variable) to be the starting point for the greatest number of transfers.
Lice act as vectors of blood-borne pathogens in other host species and two blood-borne pathogens found in lemurs, Babesia cheirogalei and Babesia propitheci, are known to be transmitted by ectoparasites (especially ticks) . It remains to be determined if L. verruculosus transmits blood-borne pathogens. Microcebus spp. are found throughout the island of Madagascar and often come into close contact with humans through a combination of anthropogenic habitat destruction and their generalist behavior; thus it is potentially beneficial to understand their parasite ecology and its implications not only for their population but for other species, including humans, as well.
Beldomenico and Begon  proposed that animals with poor body conditions are more susceptible to parasitic/pathogenic infections, which in turn would perpetuate their poor body conditions. They refer to this as a 'vicious circle' which results in heavily infested animals that become 'superspreaders', who disproportionately contribute to the dispersal of parasites in a population. Our technique of following the movement of lice through a wild population revealed the presence of lemurs that did disproportionately contribute lice to the rest of the population, making them 'donors' or 'superspreaders'. However, the mouse lemurs most heavily parasitized in this study were the ones that collected the most lice from others and hence not superspreaders, but rather 'recipients' or 'supercollectors'. Heavy louse infestation may be due to poorer overall body condition; however, as is seen in Table 1 (and Additional file 10: Text S1) we found no significant trend with body mass, age or testicular volume that would suggest that the supercollectors have the poorest body conditions.
The superspreaders suggested by  as the primary carriers and distributors of parasites may make parasite populations vulnerable, as the host's poor body condition would result in an increased likelihood of being preyed upon [28–30]. We suggest that rather than superspreaders simultaneously occurring as heavily infested supercollectors, the presence of both types of individuals occur independently in wild populations. Perhaps with further research tracking parasites in natural habitats, alternate disease dispersal routes will be revealed.