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.

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.

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.

When cold is better: climate-driven elevation shifts yield complex patterns of diversification and demography in an alpine specialist (American pika, Ochotona princeps).

The genetic consequences of climate-driven range fluctuation during the Pleistocene have been well studied for temperate species, but cold-adapted (e.g., alpine, arctic) species that may have responded uniquely to past climatic events have received less attention. In particular, we have no a priori expectation for long-term evolutionary consequences of elevation shifts into and out of sky islands by species adapted to alpine habitats. Here, we examined the influence of elevation shifts on genetic differentiation and historical demography in an alpine specialist, the American pika (Ochotona princeps). Pika populations are divided into five genetic lineages that evolved in association with separate mountain systems, rather than lineages that reflect individual sky islands. This suggests a role for glacial-period elevation shifts in promoting gene flow among high-elevation populations and maintaining regional cohesion of genetic lineages. We detected a signature of recent demographic decline in all lineages, consistent with the expectation that Holocene climate warming has driven range retraction in southern lineages, but unexpected for northern populations that presumably represent postglacial expansion. An ecological niche model of past and future pika distributions highlights the influence of climate on species range and indicates that the distribution of genetic diversity may change dramatically with continued climate warming.

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.

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.

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.