Loss of genetic diversity, recovery and allele surfing in a colonizing parasite, Geomydoecus aurei.

Understanding the genetic consequences of changes in species distributions has wide-ranging implications for predicting future outcomes of climate change, for protecting threatened or endangered populations and for understanding the history that has led to current genetic patterns within species. Herein, we examine the genetic consequences of range expansion over a 25-year period in a parasite (Geomydoecus aurei) that is in the process of expanding its geographic range via invasion of a novel host. By sampling the genetics of 1,935 G. aurei lice taken from 64 host individuals collected over this time period using 12 microsatellite markers, we test hypotheses concerning linear spatial expansion, genetic recovery time and allele surfing. We find evidence of decreasing allelic richness (AR) with increasing distance from the source population, supporting a linear, stepping stone model of spatial expansion that emphasizes the effects of repeated bottleneck events during colonization. We provide evidence of post-bottleneck genetic recovery, with average AR of infrapopulations increasing about 30% over the 225-generation span of time observed directly in this study. Our estimates of recovery rate suggest, however, that recovery has plateaued and that this population may not reach genetic diversity levels of the source population without further immigration from the source population. Finally, we employ a grid-based sampling scheme in the region of ongoing population expansion and provide empirical evidence for the power of allele surfing to impart genetic structure on a population, even under conditions of selective neutrality and in a place that lacks strong barriers to gene flow.

Using museum pelt collections to generate pollen prints from high-risk regions: A new palynological forensic strategy for geolocation.

The use of pollen as a forensic tool for geolocation is a well-established practice worldwide in cases ranging from the provenance of drugs and other illicit materials to tracking the travel of individuals in criminal investigations. Here we propose a novel approach to generation of pollen databases that uses pollen vacuumed from mammal pelts collected historically from international areas that are now deemed too high risk to visit. We present the results of a study we conducted using mammal pelts collected from Mexico. This new investigative technique is important because, although it would seem that the ubiquitous and geo-specific nature of pollen would make pollen analysis among the most promising forensic tools for law enforcement and intelligence agencies, it is not the case. The process is notoriously slow because pollen identification is a tedious task requiring trained specialists (palynologists) who are few in number worldwide, and the reference materials necessary for geolocation usually are rare or absent, especially from regions of the world that are no longer safe to visit because of war or threat of terrorism. Current forensic palynological work is carried out by a few highly trained palynologists who require accurate databases of pollen distribution, especially from sensitive areas, to do their jobs accurately and efficiently. Our project shows the suitability of using the untapped museum pelt resources to support homeland security programs. This first palynological study using museum pelts yielded 133 different pollen and spore types, including 8 moss or fern families, 12 gymnosperm genera and 112 angiosperm species. We show that the palynological print from each region is statistically different with some important clustering, demonstrating the potential to use this technique for geolocation.

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.

Tactile discriminatory ability and foraging strategies in Kangaroo rats and pocket mice (Rodentia: Heteromyidae).

A comparative study of seasonal food hoarding activity and tactile discriminatory ability in four species of heteromyid rodents (Dipodomys panamintinus, D. merriami, Perognathus longimembris, and P. formosus) was conducted in laboratory test arenas. Animals were tested individually to determine their treatment of seed (white millet) and seed mimics (glass beads and gravel) offered as food. In general, all animals showed low levels of millet hoarding activity during winter months with higher levels in fall and spring. Observations revealed that all species manipulated (with the forepaws) each potential food item prior to eating, pouching, or rejecting it. These tactile cues appear to surpass visual and olfactory cues as critical factors in distinguishing between food and food mimics. Pocket mice (Perognathus) showed high levels of tactile discriminatory ability which may serve as the mechanism by which they achieve high foraging efficiency in nature when "filter-feeding" for widely dispersed seed resources. Kangaroo rats (Dipodomys), on the other hand, are less adept at distinguishing between food and very similar non-food items. The fact that, in nature, kangaroo rats depend heavily on clumped food resources may obviate the need for highly efficient tactile discriminatory abilities.

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.

Codivergence in heteromyid rodents (Rodentia: heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: anoplura).

Although most studies of codivergence rely primarily on topological comparisons of host and parasite phylogenies, temporal assessments are necessary to determine if divergence events in host and parasite trees occurred contemporaneously. A combination of cophylogenetic analyses and comparisons of branch lengths are used in this study to understand the host-parasite association between heteromyid rodents (Rodentia: Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: Anoplura). Cophylogenetic comparisons based on nucleotide substitutions in the mitochondrial COI gene reveal a significant, but not perfect, pattern of cophylogeny between heteromyids and their sucking lice. Regression analyses show a significant functional relationship between the lengths of analogous branches in the host and parasite trees, indicating that divergence events in hosts and parasites were approximately contemporaneous. Thus, the topological similarity observed between heteromyids and their lice is the result of codivergence. These analyses also show that the COI gene in lice is evolving two to three times faster than the same gene in their hosts (similar to the results of studies of other lice and their vertebrate hosts) and that divergence events in lice occurred shortly after host divergence. We recommend that future studies of codivergence include temporal comparisons and, when possible, use the same molecular marker(s) in hosts and parasites to achieve the greatest insight into the history of the host-parasite relationship.

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.

Threat of hantavirus pulmonary syndrome to field biologists working with small mammals.

Low risk for hantavirus pulmonary syndrome (HPS) has been reported among biologists engaged in fieldwork with rodents. The overall probability of acquiring HPS when working with rodents appears to be 1 in 1,412 (0.00071). Nonetheless, a causal link between HPS and lack of personal protective equipment (PPE) use is suggested by some investigators. However, supporting data are incomplete and consequently misleading. A recent HPS case was assumed to be acquired during rodent-handling activities, although substantial peridomestic exposure was evident. Regulatory groups interpret inadequate data as evidence of the need for excessive and inappropriate PPE, which can hamper field research and instructional efforts. PPE recommendations should be reviewed and revised to match the risk associated with different types of fieldwork with small mammals.

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 (H̄ = 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 FST = 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 (FST = 0.240) was similar to that measured among host populations (FST = 0.236), suggesting a close association between gene flow in pocket gophers and gene flow in their lice.

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.

Systematics and phylogeography of pocket gophers in the genera Cratogeomys and Pappogeomys.

Mitochondrial-DNA sequence data were analyzed from individuals sampled from 38 localities across the complete geographic range of the closely related pocket gopher genera Pappogeomys and Cratogeomys. Results of phylogenetic analysis of 1133 base pairs from the cytochrome b gene are consistent with past hypotheses of relationships among members of the castanops species group within the genus Cratogeomys. However, phylogeographic variation within the gymnurus species group of the genus Cratogeomys differs significantly from relationships reflected by current taxonomy. The data indicate that there are five geographically distinct clades within the gymnurus species group. Members of the two nominal species C. gymnurus and C. tylorhinus are scattered among these clades. The three peripherally isolated species, C. fumosus, C. neglectus, and C. zinseri, do not appear to be genetically distinct from other gymnurus species group taxa. An historical biogeographic hypothesis is proposed that will be tested using nuclear DNA data.