Cophylogeny on a fine scale: Geomydoecus chewing lice and their pocket gopher hosts, Pappogeomys bulleri

Many species of pocket gophers and their ectoparasitic chewing lice have broadly congruent phylogenies, indicating a history of frequent codivergence. For a variety of reasons, phylogenies of codiverging hosts and parasites are expected to be less congruent for more recently diverged taxa. This study is the first of its scale in the pocket gopher and chewing louse system, with its focus entirely on comparisons among populations within a single species of host and 3 chewing louse species in the Geomydoecus bulleri species complex. We examined mitochondrial DNA from a total of 46 specimens of Geomydoecus lice collected from 11 populations of the pocket gopher host, Pappogeomys bulleri. We also examined nuclear DNA from a subset of these chewing lice. Louse phylogenies were compared with a published pocket gopher phylogeny. Contrary to expectations, we observed a statistically significant degree of parallel cladogenesis in these closely related hosts and their parasites. We also observed a higher rate of evolution in chewing louse lineages than in their corresponding pocket gopher hosts. In addition, we found that 1 louse species (Geomydoecus burti) may not be a valid species, that subspecies within G. bulleri are not reciprocally monophyletic, and that morphological and genetic evidence support recognition of a new species of louse, Geomydoecus pricei.     

Comparative body size relationships in pocket gophers and their chewing lice

In this paper, we use the method of independent contrasts to study body size relationships between pocket gophers and their chewing lice, a host-parasite system in which both host and parasite phylogcnies are well studied. The evolution of body size of chewing lice appears to be dependent only on the body size of their hosts, which confirms the 1991 findings of Harvey and Keymer. We show that there is a positive relationship between body size and hair-shaft diameter in pocket gophers, and that there is also a positive relationship between body size and head-groove width in chewing lice. Finally, we show a positive relationship between gopher hair-shaft diameter and louse head-groove width. We postulate that changes in body size of chewing lice are driven by a mechanical relationship between the parasite's head-groove dimension and the diameter of the hairs of its host. Louse species living"on larger host species may be larger simply because their hosts have thicker hairs, which requires that the lice have a wider head groove. Our study of gopher hair-shaft diameter and louse head-groove dimensions suggest that there is a 'lock-and-key' relationship between these two anatomical features.     

Temporal and spatial dynamics of competitive parapatry in chewing lice

We synthesize observations from 1979 to 2016 of a contact zone involving two subspecies of pocket gophers (Thomomys bottae connectens and T. b. opulentus) and their respective chewing lice (Geomydoecus aurei and G. centralis) along the Río Grande Valley in New Mexico, U.S.A., to test predictions about the dynamics of the zone. Historically, the natural flood cycle of the Rio Grande prevented contact between the two subspecies of pocket gophers. Flood control measures completed in the 1930s permitted contact, thus establishing the hybrid zone between the pocket gophers and the contact zone between their lice (without hybridization). Since that time, the pocket gopher hybrid zone has stabilized, whereas the northern chewing louse species has replaced the southern louse species at a consistent rate of ~150 m/year. The 0.2–0.8 width of the replacement zone has remained constant, reflecting the constant rate of chewing louse species turnover on a single gopher and within a local pocket gopher population. In contrast, the full width of the replacement zone (northernmost G. centralis to southernmost G. aurei) has increased annually. By employing a variety of metrics of the species replacement zone, we are better able to understand the dynamics of interactions between and among the chewing lice and their pocket gopher hosts. This research provides an opportunity to observe active species replacement and resulting distributional shifts in a parasitic organism in its natural setting.     

Phylogenetic analysis of bacterial communities associated with ectoparasitic chewing lice of pocket gophers: a culture-independent approach

This study identifies the bacteria associated with ectoparasitic chewing lice that live in the fur of pocket gophers. Samples of chewing lice were collected from pocket gopher hosts in Florida, Missouri, New Mexico, and Costa Rica. We used a molecular sampling method whereby total community DNA was extracted from samples of chewing lice, and PCR was used to selectively amplify small-subunit rRNA genes from bacteria. This culture-independent method yielded ca. 35 distinct lineages representing eight widely divergent groups within the domain Bacteria. Phylogenetic analysis of two lineages (Acinetobacter and Staphylococcus) provides evidence that multiple species of each group are found in chewing lice. Phylogenetic analysis also demonstrated that diversification within chewing lice may be evident in both Acinetobacter and Staphylococcus. Some clones amplified from chewing louse hosts appeared to be distinct from known species of Acinetobacter and Staphylococcus. This diversification may be the result of the extreme isolation of populations of both chewing lice and their pocket gopher hosts.     

Pocket gophers and chewing lice: a test of the maternal transmission hypothesis

The life-history traits of pocket gophers and their chewing lice suggest that there is little opportunity for transmission of parasites among pocket gophers, with the exception of transmission from mother to offspring. Herein, we test the hypothesis that lice are transmitted maternally by using an indirect approach that compares the distribution of louse populations to the distribution of mitochondrial DNA haplotypes in the pocket gophers. Comparison of the chewing louse distributions to the distribution of mtDNA haplotypes for the gophers revealed no significant concordance, and thus falsifies the maternal transmission hypothesis.     

Host shift and cospeciation rate estimation from co‐phylogenies

Host shifts can cause novel infectious diseases, and is a key process in diversification. Disentangling the effects of host shift vs. those of cospeciation is non‐trivial as both can result in phylogenic congruence. We develop a new framework based on network analysis and Approximate Bayesian Computation to quantify host shift and cospeciation rates in host‐parasite systems. Our method enables estimation of the expected time to the next host shift or cospeciation event. We then apply it to avian haemosporidian parasite systems and to the pocket gophers‐chewing lice system, and demonstrate that both host shift and cospeciation can be reliably estimated by our method. We confirm that host shifts have shaped the evolutionary history of avian haemosporidian parasites and have played a minor role in the gopher–chewing lice system. Our method is promising for predicting the rate of potential host shifts and thus the emergence of novel infectious diseases.     

GENETIC DIFFERENTIATION AMONG CHEWING LOUSE POPULATIONS (MALLOPHAGA: TRICHODECTIDAE) IN A POCKET GOPHER CONTACT ZONE (RODENTIA: GEOMYIDAE)

Genetic variation among populations of chewing lice (Geomydoecus actuosi) was examined in relation to chromosomal and electrophoretic variation among populations of their hosts (Thomomys bottae) at a contact zone. Louse demes were characterized by low levels of genetic heterozygosity (H? = 0.039) that may result from founder effects during primary infestation of hosts, compounded by seasonal reductions in louse population size. Louse populations sampled from different hosts showed high levels of genetic structuring both within and among host localities. Microgeographic differentiation of louse populations is high (mean F_ST = 0.092) suggesting that properties of this host–parasite system promote differentiation of louse populations living on different individual hosts. Among-population differentiation in lice (F_ST = 0.240) was similar to that measured among host populations (F_ST = 0.236), suggesting a close association between gene flow in pocket gophers and gene flow in their lice.     

Biogeography explains cophylogenetic patterns in toucan chewing lice

Historically, comparisons of host and parasite phylogenies have concentrated on cospeciation. However, many of these comparisons have demonstrated that the phylogenies of hosts and parasites are seldom completely congruent, suggesting that phenomena other than cospeciation play an important role in the evolution of host-parasite assemblages. Other coevolutionary phenomena, such as host switching, parasite duplication (speciation on the host), sorting (extinction), and failure to speciate can also influence host-parasite assemblages. Using mitochondrial and nuclear protein-coding DNA sequences, I reconstructed the phylogeny of ectoparasitic toucan chewing lice in the Austrophilopterus cancellosus subspecies complex and compared this phylogeny with the phylogeny of the hosts, the Ramphastos toucans, to reconstruct the history of coevolutionary events in this host-parasite assemblage. Three salient findings emerged. First, reconstructions of host and louse phylogenies indicate that they do not branch in parallel, and their cophylogenetic history shows little or no significant cospeciation. Second, members of monophyletic Austrophilopterus toucan louse lineages are not necessarily restricted to monophyletic host lineages. Often, closely related lice are found on more distantly related but sympatric toucan hosts. Third, the geographic distribution of the hosts apparently plays a role in the speciation of these lice. These results suggest that for some louse lineages biogeography may be more important than host associations in structuring louse populations and species, particularly when host life history (e.g., hole nesting) or parasite life history (e.g., phoresis) might promote frequent host switching events between syntopic host species. These findings highlight the importance of integrating biogeographic information into cophylogenetic studies.     

Phylogeny of Geomydoecus and Thomomydoecus pocket gopher lice (Phthiraptera: Trichodectidae) inferred from cladistic analysis of adult and first instar morphology

The phylogeny for all 122 species and subspecies of chewing lice of the genera Geomydoecus and Thomomydoecus (Phthiraptera: Trichodectidae) hosted by pocket gophers (Rodentia: Geomyidae) is estimated by a cladistic analysis of fifty-eight morphological characters obtained from adults and first instars. The data set has considerable homoplasy, but still contains phylogenetic information. The phylogeny obtained is moderately resolved and, with some notable exceptions, supports the species complexes proposed by Hellenthal and Price over the the last two decades. The subgenera G. (Thaelerius) and T. (Thomomydoecus) are both shown to be monophyletic, but the monophly of subgenus T. (Jamespattonius) could not be confirmed, perhaps due to the lack of first-instar data for one of its component species. The nominate subgenus of Geomydoecus may be monophyletic, but our cladogram was insufficiently resolved to corroborate this. Mapping the pocket gopher hosts onto the phylogeny reveals a consistent pattern of louse clades being restricted to particular genera or subgenera of gophers, but the history of the host-parasite association appears complex and will require considerable effort to resolve.     

Cophylogeny and disparate rates of evolution in sympatric lineages of chewing lice on pocket gophers

Although molecular-based phylogenetic studies of hosts and parasites are increasingly common in the literature, no study to date has examined two congeneric lineages of parasites that live in sympatry on the same lineage of hosts. This study examines phylogenetic relationships among chewing lice (Phthiraptera: Trichodectidae) of the Geomydoecus coronadoi and Geomydoecus mexicanus species complexes and compares these to phylogenetic patterns in their hosts (pocket gophers of the rodent family Geomyidae). Sympatry of congeneric lice provides a natural experiment to test the hypothesis that closely related lineages of parasites will respond similarly to the same host. Sequence data from the mitochondrial COI and the nuclear EF-1alpha genes confirm that the two louse complexes are reciprocally monophyletic and that individual clades within each species complex parasitize a different species of pocket gopher. Phylogenetic comparisons reveal that both louse complexes show a significant pattern of cophylogeny with their hosts. Comparisons of rates of nucleotide substitution at 4-fold degenerate sites in the COI gene indicate that both groups of lice have significantly higher basal mutation rates than their hosts. The two groups of lice have similar basal rates of mutation, but lice of the G. coronadoi complex show significantly elevated rates of nucleotide substitution at all sites. These rate differences are hypothesized to result from population-level phenomena, such as effective population size, founder effects, and drift, that influence rates of nucleotide substitution.     

STATISTICAL TESTS OF HOST-PARASITE COSPECIATION

A history of cospeciation (synchronous speciation) among ecologically associated, but otherwise distantly related, species is often revealed by a strong correspondence of their phylogenies. In this paper, we present several tests of cospeciation that use maximum-likelihood and Bayesian methods of phylogenetic estimation. The hypotheses tested include: (1) topological agreement of phylogenies for coevolving groups; (2) identical speciation times of associated species; and (3) identical evolutionary rates in genes of associated species. These tests are applied to examine a possible instance of host-parasite coevolution among pocket gophers and lice using mitochondrial COI DNA sequences. The observed differences between gopher and louse trees cannot be explained by sampling error and are consistent with a rate of host switching about one-third the host speciation rate. A subset of the gopher-louse data is consistent with a common history of evolution (i.e., the topologies and speciation times are identical). However, the relative rate of nucleotide substitution is two to four times higher in the lice than in the gophers.     

AGE AND MOVEMENT OF A HYBRID ZONE: IMPLICATIONS FOR DISPERSAL DISTANCE IN POCKET GOPHERS AND THEIR CHEWING LICE

Historical flood records for the Rio Grande Valley of New Mexico suggest that a pocket gopher (Thomomys bottae) hybrid zone previously thought to be 10,000 years old may actually be closer to 50 years old. Measured zone width (defined genetically) is consistent with the hypothesis of recent contact, if we assume a reasonable dispersal distance of approximately 400 m/year for pocket gophers. A five-year study of movement of the contact zone between the two species of chewing lice that parasitize these pocket gophers also is consistent with the hypothesis of recent origin of the zone.     

Influence of host ecology and morphology on the diversity of Neotropical bird lice

Host‐parasite systems can be powerful arenas in which to explore factors influencing community structure. We used a comparative approach to examine the influence of host ecology and morphology on the diversity of chewing lice (Insecta: Phthiraptera) among 52 species of Peruvian birds. For each host species we calculated two components of parasite diversity: 1) cumulative species richness, and 2) mean abundance. We tested for correlations between these parasite indices and 13 host ecological and morphological variables. Host ecological variables included geographic range size, local population density, and microhabitat use. Host morphological variables included body mass, plumage depth, and standard dimensions of bill, foot and toenail morphology, all of which could influence the efficiency of anti‐parasite grooming. Data were analysed using statistical and comparative methods that control for sampling effort and host phylogeny. None of the independent host variables correlated with louse species richness when treated as a dependent variable. When richness was treated as an independent variable, however, it was positively correlated with mean louse abundance. Host body mass was also positively correlated with mean louse abundance. When louse richness and host body mass were held constant, mean louse abundance correlated negatively with the degree to which the upper mandible of the host's bill overhangs the lower mandible. This correlation suggests that birds with longer overhangs are better at controlling lice during preening. We propose a specific functional hypothesis in which preening damages lice by exerting a shearing force between the overhang and the tip of the lower mandible. This study is the first to suggest a parasite‐control function of such a detailed component of bill morphology across species. Avian biologists have traditionally focused almost exclusively on bills as tools for feeding. We suggest that the adaptive radiation of bill morphology should be reinterpreted with both preening and feeding in mind.     

Lousy grouse: Comparing evolutionary patterns in Alaska galliform lice to understand host evolution and host–parasite interactions

Understanding both sides of host–parasite relationships can provide more complete insights into host and parasite biology in natural systems. For example, phylogenetic and population genetic comparisons between a group of hosts and their closely associated parasites can reveal patterns of host dispersal, interspecies interactions, and population structure that might not be evident from host data alone. These comparisons are also useful for understanding factors that drive host–parasite coevolutionary patterns (e.g., codivergence or host switching) over different periods of time. However, few studies have compared the evolutionary histories between multiple groups of parasites from the same group of hosts at a regional geographic scale. Here, we used genomic data to compare phylogenomic and population genomic patterns of Alaska ptarmigan and grouse species (Aves: Tetraoninae) and two genera of their associated feather lice: Lagopoecus and Goniodes. We used whole‐genome sequencing to obtain hundreds of genes and thousands of single‐nucleotide polymorphisms (SNPs) for the lice and double‐digest restriction‐associated DNA sequences to obtain SNPs from Alaska populations of two species of ptarmigan. We found that both genera of lice have some codivergence with their galliform hosts, but these relationships are primarily characterized by host switching and phylogenetic incongruence. Population structure was also uncorrelated between the hosts and lice. These patterns suggest that grouse, and ptarmigan in particular, share habitats and have likely had historical and ongoing dispersal within Alaska. However, the two genera of lice also have sufficient dissimilarities in the relationships with their hosts to suggest there are other factors, such as differences in louse dispersal ability, that shape the evolutionary patterns with their hosts.     

Molecular phylogeny and novel host associations of avian chewing lice (Insecta: Phthiraptera) from South Africa

Compared with Europe and the Americas, the ectoparasites of African birds are poorly understood, despite the avian fauna being relatively well known. Notably, previous studies documenting the host associations and genetic diversity of parasitic chewing lice of southern African birds have been limited in geographic and taxonomic scope. Recent field expeditions exploring the avian diversity in South Africa facilitated an opportunity to obtain louse specimens from a taxonomically diverse host assemblage. This study is the first to investigate avian louse host associations and diversity across a large portion of South Africa encompassing several distinct habitat types, while incorporating molecular genetic data (from portions of the mitochondrial COI and nuclear EF‐1α genes) for ectoparasite phylogenetic analyses. From 1105 South African bird individuals and 170 species examined for lice, a total of 105 new louse–host associations were observed. Morphological and genetic examination of lice with these new host associations reveals a maximum of 66 louse species new to science. Results of this study support the observation that examining museum specimens is a useful way to investigate louse diversity and host associations.     

Evolutionary and ecological response of pocket gophers (Thomomys talpoides) to late-Holocene climatic change

Late-Holocene evolutionary and ecological response of pocket gophers ( Thomomys talpoides ) and other species to climatic change is documented by mammalian fossils from Lamar Cave, a palaeontological site in northern Yellowstone National Park. Pocket gophers illustrate ecological sensitivity to a series of mesic to xeric climatic excursions in the sagebrush-grassland ecotone during the last 3200 years, increasing in abundance during mesic intervals, and declining in abundance during xeric intervals. Four other small mammal taxa (Microtus sp., Peromyscus maniculatus, Neotoma cinerea and Spermophilus armatus) also show response to climatic change, increasing or decreasing in abundance in accordance with their preferred habitat requirements. To determine evolutionary response to climate, two craniodental characters for the northern pocket gopher ( Thomomys talpoides ) are investigated in modern representatives within a 400 km radius of Lamar Cave and then tracked through the time spanned by the fossils. One morphologic character shows that variation in body size, primarily a plastic response to the environment, demonstrates few taxonomically consistent patterns of geographic variation across 39 modern localities. In contrast, the other character indicates genetic relatedness within subspecies. Stasis in the genetically controlled character indicates that the same subspecies of pocket gopher ( T. talpoides tenellus ) has occupied northern Yellowstone for at least 3200 years. However, T. t. tenellus does show plastic response to climatic change because pocket gophers during the Medieval Warm Period were smaller than at any other time spanned by the deposit.     

Spatial partitioning of host habitat by chewing lice of the genera Geomydoecus and Thomomydoecus (Phthiraptera: Trichodectidae)

Chewing lice, Geomydoecus and Thomomydoecus, coexist on pocket gophers, Thomomys spp. We investigated the spatial distribution of the 2 genera on their hosts and explored possible mechanisms of resource partitioning by chewing lice. Chewing lice appear to partition available host resources spatially, with Geomydoecus occurring primarily on the lateral and dorsal regions of the host, and Thomomydoecus occurring primarily on the lateral and ventral regions. Although spatial partitioning of the host habitat is evident, it does not appear to be explained by hair diameter. Spatial partitioning of the host's body could be the result of some other factor, possibly temperature or humidity gradients of the host's body.     

Rodent louse diversity,phylogeny, and cospeciation in the Manu Biosphere Reserve,Peru

We investigated the diversity, cophylogenetic relationships, and biogeography of hoplopleurid sucking lice (Phthiraptera: Anoplura) parasitizing rodents (Muridae: Sigmodontinae) in the Manu National Park and Biosphere Reserve. Our morphological and molecular studies reveal that 15 distinct louse species parasitize 19 rodent species. Three of these louse species are new to science, and all but two of the host associations were previously unknown. We find that hoplopleurid lice in South America parasitize multiple host species across a large geographic area, and that Peru represents a new geographic locality for almost all the louse species collected in the present study. Phylogenetic analyses of mitochondrial and nuclear data reveal that the louse family Hoplopleuridae and the genera Hoplopleura and Pterophthirus are not monophyletic, and lice do not appear to group by host tribe, collecting locality, or collection elevation. The lack of monophyly for these apparently natural groups (taxonomic, locality, and elevation) indicates that host switching with or without parasite speciation may be prevalent among hoplopleurid lice. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 598–610.     

Population biology of swift (Apus apus) ectoparasites in relation to host reproductive success

Abstract.

• 1 We censused ectoparasite populations of adult and nestling swifts over the course of the host's breeding season. Nearly all of the birds were infested with chewing lice and two-thirds of the nests were infested with louse flies. Feather mites were observed but not quantified.
• 2 Lice and louse flies both showed aggregated distributions among hosts. Louse eggs, hatched lice and adult louse flies had negative binomial distributions, whereas the aggregated distribution of louse fly pupae was not adequately described by negative binomial or Poisson models.
• 3 Transmission of lice from parents to offspring was documented. A comparison of the age structure of lice on parents and offspring indicated that most transmission was by nymphal lice.
• 4 Host reproductive success and survival appeared to be independent of the number of lice or louse flies. Neither parasite correlated with the number, body mass, or date of fledging of young birds, nor with the overwinter survival of adults. We caution, however, that experimental manipulations of parasite load are required for a definitive test of the impact of ectoparasites on evolutionary fitness components.

     

AVIAN BROOD PARASITISM AND ECTOPARASITE RICHNESS–SCALE‐DEPENDENT DIVERSITY INTERACTIONS IN A THREE‐LEVEL HOST–PARASITE SYSTEM

Brood parasitic birds, their foster species and their ectoparasites form a complex coevolving system composed of three hierarchical levels. However, effects of hosts’ brood parasitic life‐style on the evolution of their louse (Phthiraptera: Amblycera, Ischnocera) lineages have never been tested. We present two phylogenetic analyses of ectoparasite richness of brood parasitic clades. Our hypothesis was that brood parasitic life‐style affects louse richness negatively across all avian clades due to the lack of vertical transmission routes. Then, narrowing our scope to brood parasitic cuckoos, we explored macroevolutionary factors responsible for the variability of their louse richness. Our results show that taxonomic richness of lice is lower on brood parasitic clades than on their nonparasitic sister clades. However, we found a positive covariation between the richness of cuckoos’ Ischnoceran lice and the number of their foster species, possibly due to the complex and dynamic subpopulation structure of cuckoo species that utilize several host species. We documented diversity interactions across a three‐level host parasite system and we found evidence that brood parasitism has opposing effects on louse richness at two slightly differing macroevolutionary scales, namely the species richness and the genera richness.