Coevolving histories inside and out: phylogenetics, comparative parasitology, and host affinities of chipmunk sucking lice and pinworms

Diversification of parasite species, in light of their host association, is an area ripe for testing hypotheses of evolution when one species requires another for survival. The 23 species of western North American chipmunks (genus Tamias) host two species of ectoparasitic sucking lice (Anoplura) and two species of endoparasitic pinworms (Nematoda). I used a phylogenetic approach to investigate the evolutionary histories of the parasites in light of the hosts and the landscape. In comparing the parasites, I found that the two pinworm species have similar diversification patterns, linked to hosts, but those processes occurred on different time scales. As another paired investigation, the chipmunk sucking lice revealed some lineages that correspond to host relationships, but the lice have different histories from the hosts, as well as each other. Overall, this system demonstrates that parasite diversification cannot be explained as a simple process of codivergence and that parasite evolution, even when comparing parasites from the same hosts and ecological roles, is complex and the history is unique to each species. While I found a role for hosts, host demographic history, and landscape in shaping genetic structure in all four parasites, these processes impacted each parasite species differently

Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites.

Museum specimens play an increasingly important role in predicting the outcomes and revealing the consequences of anthropogenically driven disruption of the biosphere. As ecological communities respond to ongoing environmental change, host-parasite interactions are also altered. This shifting landscape of host-parasite associations creates opportunities for colonization of different hosts and emergence of new pathogens, with implications for wildlife conservation and management, public health, and other societal concerns. Integrated archives that document and preserve mammal specimens along with their communities of associated parasites and ancillary data provide a powerful resource for investigating, anticipating, and mitigating the epidemiological, ecological, and evolutionary impacts of environmental perturbation. Mammalogists who collect and archive mammal specimens have a unique opportunity to expand the scope and impact of their field work by collecting the parasites that are associated with their study organisms. We encourage mammalogists to embrace an integrated and holistic sampling paradigm and advocate for this to become standard practice for museum-based collecting. To this end, we provide a detailed, field-tested protocol to give mammalogists the tools to collect and preserve host and parasite materials that are of high quality and suitable for a range of potential downstream analyses (e.g., genetic, morphological). Finally, we also encourage increased global cooperation across taxonomic disciplines to build an integrated series of baselines and snapshots of the changing biosphere. Los especímenes de museo desempeñan un papel cada vez más importante tanto en la descripción de los resultados de la alteración antropogénica de la biosfera como en la predicción de sus consecuencias. Dado que las comunidades ecológicas responden al cambio ambiental, también se alteran las interacciones hospedador-parásito. Este panorama cambiante de asociaciones hospedador-parásito crea oportunidades para la colonización de diferentes hospedadores y para la aparición de nuevos patógenos, con implicancias en la conservación y manejo de la vida silvestre, la salud pública y otras preocupaciones de importancia para la sociedad. Archivos integrados que documentan y preservan especímenes de mamíferos junto con sus comunidades de parásitos y datos asociados, proporcionan un fuerte recurso para investigar, anticipar y mitigar los impactos epidemiológicos, ecológicos y evolutivos de las perturbaciones ambientales. Los mastozoólogos que recolectan y archivan muestras de mamíferos, tienen una oportunidad única de ampliar el alcance e impacto de su trabajo de campo mediante la recolección de los parásitos que están asociados con los organismos que estudian. Alentamos a los mastozoólogos a adoptar un paradigma de muestreo integrado y holístico y abogamos para que esto se convierta en una práctica estándarizada de la obtención de muestras para museos. Con este objetivo, proporcionamos un protocolo detallado y probado en el campo para brindar a los mastozoólogos las herramientas para recolectar y preservar materiales de parásitos y hospedadores de alta calidad y adecuados para una gran variedad de análisis subsecuentes (e.g., genéticos, morfológicos, etc.). Finalmente, también abogamos por una mayor cooperación global entre las diversas disciplinas taxonómicas para construir una serie integrada de líneas de base y registros actuales de nuestra cambiante biosfera

Data from: Sympatric parasites have similar host-associated, but asynchronous, patterns of diversification

Parasitism is a common symbiotic interaction across diverse natural systems. Using a comparative evolutionary approach, we investigated the contributions of both host phylogeny and abiotic factors towards diversification of phylogenetically independent endoparasites that inhabit essentially the same physical space. We tested for host-parasite and parasite-parasite phylogenetic concordance in western North American chipmunks (Rodentia: Sciuridae) and two distantly related species of pinworms (Nematoda: Oxyurida). Deep structure in molecular phylogenies revealed signals of host-associated divergence in both parasite species, while shallower phylogeographic structure varied between the two parasites. This suggests that although these parasites experienced similar landscapes and cyclic climate processes, temporally distinctive diversification events were associated with differences in the initiation of their association with host lineages. When climate cycles initiate diversification, partially congruent, but asynchronous host-associated parasite phylogenies may emerge

Pinworm & host BUCKy trees and pinworm COI BEAST tree

H_cucullatum_COI_quadrivittatus_cytb_BUCKy.tre: BUCKy tree with concordance values for H. cucullatum COI MrBayes trees and quadrivittatus group cytb MrBayes trees H_cucullatum_R_eutamii_COI_BUCKy.tre: BUCKy tree with concordance values for H. cucullatum and R. eutamii COI MrBayes trees H_cucullatum_and_R_eutamii_COI_beast_rate_estimates_only.tre: BEAST tree of COI sequences for H. cucullatum and R. eutamii, used only to estimate relative rates H_cucullatum_COI_T_minimus_cytb_BUCKy.tre: BUCKy tree with concordance values for H. cucullatum COI MrBayes trees and T. minimus cytb MrBayes trees R_eutamii_COI_T_minimus_cytb_BUCKy.tre: BUCKy tree with concordance values for R. eutamii COI MrBayes trees and T. minimus cytb MrBayes trees R_eutamii_COI_quadrivittatus_cytb_BUCKy.tre: BUCKy tree with concordance values for R. eutamii COI MrBayes trees and quadrivittatus group cytb MrBayes tree

Heteroxynema cucullatum DNA sequence alignments and phylogenies

H_cucullatum_3loci_concatenated_MrBayes.tre: MrBayes tree of Heteroxynema cucullatum concatenated loci COI, ITS+, 28S H_cucullatum_3loci_starbeast.tre: Starbeast species tree of Heteroxynema cucullatum loci COI, ITS+, 28S H_cucullatum_COI_quadrivittatus_hosts_MrBayes.tre: MrBayes gene tree of COI for Heteroxynema cucullatum individuals that corespond to quadrivittatus group hosts (used in tanglegram) H_cucullatum_COI_T_minimus_hosts_MrBayes.tre: MrBayes gene tree of COI for Heteroxynema cucullatum individuals that corespond to Tamias minimus hosts (used in tanglegram) Heteroxynema_cucullatum_28S_MrBayes.tre: MrBayes gene tree of Heteroxynema cucullatum 28S Heteroxynema_cucullatum_28S_alignment.nex: DNA sequence alignment of Heteroxynema cucullatum 28S Heteroxynema_cucullatum_COI_MrBayes.tre: MrBayes gene tree of Heteroxynema cucullatum COI Heteroxynema_cucullatum_COI_RAxML.tre: RAxML gene tree of Heteroxynema cucullatum COI Heteroxynema_cucullatum_COI_alignment.nex: DNA sequence alignment of Heteroxynema cucullatum COI Heteroxynema_cucullatum_ITS_MrBayes.tre: MrBayes gene tree of Heteroxynema cucullatum ITS+ Heteroxynema_cucullatum_ITS_alignment.nex: DNA sequence alignment of Heteroxynema cucullatum ITS

Data from: Impacts of inference method and dataset filtering on phylogenomic resolution in a rapid radiation of ground squirrels (Xerinae: Marmotini)

Phylogenomic datasets are illuminating many areas of the Tree of Life. However, the large size of these datasets alone may be insufficient to resolve problematic nodes in the most rapid evolutionary radiations, because inferences in zones of extraordinarily low phylogenetic signal can be sensitive to the model and method of inference, as well as the information content of loci employed. We used a dataset of >3,950 ultraconserved element (UCE) loci from a classic mammalian radiation, ground-dwelling squirrels of the tribe Marmotini (Sciuridae: Xerinae), to assess sensitivity of phylogenetic estimates to varying per-locus information content across 4 different inference methods (RAxML, ASTRAL, NJst, SVDquartets). Persistent discordance was found in topology and bootstrap support between concatenation- and coalescent-based inferences; among methods within the coalescent framework; and within all methods in response to different filtering scenarios. Contrary to some recent empirical UCE-based studies, filtering by information content did not promote complete among-method concordance. Nevertheless, filtering did improve concordance relative to randomly selected locus sets, largely via improved consistency of two-step summary methods (particularly NJst) under conditions of higher average per-locus variation (and thus increasing gene tree precision). The benefits of dataset filtering are notably variable among classes of inference methods and across different evolutionary scenarios, reiterating the complexities of resolving rapid radiations, even with robust taxon and character sampling

Supplementary Appendix S1

.csv file containing taxonomic identities, institutional IDs, collection year, and number of UCE contigs assembled for all samples sequenced in this study data fields are synonymized with standard Darwin Core terms (https://github.com/tdwg/dwc) where possibl

Rauschtineria eutamii DNA sequence alignments and phylogenies

R_eutamii_4loci_concatenated_MrBayes.tre: MrBayes tree of Rauschtineria eutamii concatenated loci COI, 12S, 18S, 28S R_eutamii_4loci_starbeast.tre: Starbeast species tree of Rauschtineria eutamii loci COI, 12S, 18S, 28S R_eutamii_COI_minimus_hosts_MrBayes.tre: MrBayes gene tree of COI for Rauschtineria eutamii individuals that corespond to Tamias minimus hosts (used in tanglegram) R_eutamii_COI_quadrivittatus_hosts_MrBayes.tre: MrBayes gene tree of COI for Rauschtineria eutamii individuals that corespond to quadrivittatus group hosts (used in tanglegram) Rauschtineria_eutamii_12S_MrBayes.tre: MrBayes gene tree of Rauschtineria eutamii 12S Rauschtineria_eutamii_12S_alignment.nex: DNA sequence alignment of Rauschtineria eutamii 12S Rauschtineria_eutamii_18S_MrBayes.tre: MrBayes gene tree of Rauschtineria eutamii 18S Rauschtineria_eutamii_18S_alignment.nex: DNA sequence alignment of Rauschtineria eutamii 18S Rauschtineria_eutamii_28S_MrBayes.tre: MrBayes gene tree of Rauschtineria eutamii 28S Rauschtineria_eutamii_28S_alignment.nex: DNA sequence alignment of Rauschtineria eutamii 28S Rauschtineria_eutamii_COI_MrBayes.tre: MrBayes gene tree of Rauschtineria eutamii COI Rauschtineria_eutamii_COI_RAxML.tre: RAxML gene tree of Rauschtineria eutamii COI Rauschtineria_eutamii_COI_alignment.nex: DNA sequence alignment of Rauschtineria eutamii CO

Supplementary Fig. S2

Relationships of UCE variability (proportion of variable sites per locus (i.e., our metric)) with alternative metrics of information content: a) the proportion of parsimony sites per locus, b) the mean bootstrap support found in corresponding gene trees, and c) the proportion of gene tree nodes resolved with >70% bootstrap support

njst_empirical_trees

NJst species trees from empirically filtered datasets labeled with support values from 100 bootstrap replicates and rooted on Aplodontia rufa. Trees are named with the filtering level used (e.g., 5var = at least 5 percent variable sites per locus) followed by the number of resulting UCE loci in each datase