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1. Dispersal-Limited Symbionts Exhibit Unexpectedly Wide Variation in Host Specificity

   https://doi.org/10.1093/sysbio/syad014  

   Matthews, Alix_E ; Wijeratne, Asela_J ; Sweet, Andrew_D ; Hernandes, Fabio_A ; Toews, David_P_L ; Boves, Than_J ; Esposito, ed., Lauren ( March 2023 , Systematic Biology)

   A fundamental aspect of symbiotic relationships is host specificity, ranging from extreme specialists associated with only a single host species to generalists associated with many different species. Although symbionts with limited dispersal capabilities are expected to be host specialists, some are able to associate with multiple hosts. Understanding the micro- and macro-evolutionary causes of variations in host specificity is often hindered by sampling biases and the limited power of traditional evolutionary markers. Here, we studied feather mites to address the barriers associated with estimates of host specificity for dispersal-limited symbionts. We sampled feather mites (Proctophyllodidae) from a nearly comprehensive set of North American breeding warblers (Parulidae) to study mite phylogenetic relationships and host–symbiont codiversification. We used pooled-sequencing (Pool-Seq) and short-read Illumina technology to interpret results derived from a traditional barcoding gene (cytochrome c oxidase subunit 1) versus 11 protein-coding mitochondrial genes using concatenated and multispecies coalescent approaches. Despite the statistically significant congruence between mite and host phylogenies, mite–host specificity varies widely, and host switching is common regardless of the genetic marker resolution (i.e., barcode vs. multilocus). However, the multilocus approach was more effective than the single barcode in detecting the presence of a heterogeneous Pool-Seq sample. These results suggest that presumed symbiont dispersal capabilities are not always strong indicators of host specificity or of historical host–symbiont coevolutionary events. A comprehensive sampling at fine phylogenetic scales may help to better elucidate the microevolutionary filters that impact macroevolutionary processes regulating symbioses, particularly for dispersal-limited symbionts. [Codiversification; cophylogenetics; feather mites; host switching; pooled sequencing; species delineation; symbiosis, warblers.]

    

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2. Differential survival and dispersal of avian feather mites with contrasting host specificities

   https://doi.org/10.1111/een.13176  

   Matthews, Alix E. ; Barnett, Cody J. ; Boves, Than J. ( June 2022 , Ecological Entomology)

   Host specificity is a fundamental life history trait of symbionts and exists on a broad continuum from symbionts that are specific to one or a few hosts (host specialists), to those associated with multiple different host species (host generalists). However, the biological mechanisms underlying the complexity and wide variation in symbiont host specificity are poorly understood from both the symbiont and host perspectives across many symbiotic systems.

   Feather mites are common avian symbionts that vary in their host specificity from extreme host generalists to host specialists, even among species within the same genus.

   Here, we measured and compared survival probability and rate of dispersal to determine how these traits differ between two species of feather mites in the same genus: one host generalist associated with 17 host species (Amerodectes ischyros) and one host specialist with only one known host (A. protonotaria).

   We initially predicted that the host generalist would live longer and disperse more rapidly but discovered that while the host generalist mite survived longer, the host specialist mite dispersed more quickly.

   The differing environmental and ecological conditions in which the hosts of these mites are associated may explain the survival and dispersal patterns we uncovered, as differential microclimates may have led to different selective pressures on each species of mite. We also noted mite behavioural observations and suggest experiments to extend our understanding of feather mite ecology and evolution.

    

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3. The structured diversity of specialized gut symbionts of the New World army ants

   https://doi.org/10.1111/mec.14140  

   Łukasik, Piotr ; Newton, Justin A. ; Sanders, Jon G. ; Hu, Yi ; Moreau, Corrie S. ; Kronauer, Daniel J. C. ; O'Donnell, Sean ; Koga, Ryuichi ; Russell, Jacob A. ( May 2017 , Molecular Ecology)

   Symbiotic bacteria play important roles in the biology of their arthropod hosts. Yet the microbiota of many diverse and influential groups remain understudied, resulting in a paucity of information on the fidelities and histories of these associations. Motivated by prior findings from a smaller scale, 16SrRNA‐based study, we conducted a broad phylogenetic and geographic survey of microbial communities in the ecologically dominant New World army ants (Formicidae: Dorylinae). Amplicon sequencing of the 16SrRNAgene across 28 species spanning the five New World genera showed that the microbial communities of army ants consist of very few common and abundant bacterial species. The two most abundant microbes, referred to as Unclassified Firmicutes and Unclassified Entomoplasmatales, appear to be specialized army ant associates that dominate microbial communities in the gut lumen of three host genera,Eciton,LabidusandNomamyrmex. Both are present in other army ant genera, including those from the Old World, suggesting that army ant symbioses date back to the Cretaceous. Extensive sequencing of bacterial protein‐coding genes revealed multiple strains of these symbionts coexisting within colonies, but seldom within the same individual ant. Bacterial strains formed multiple host species‐specific lineages on phylogenies, which often grouped strains from distant geographic locations. These patterns deviate from those seen in other social insects and raise intriguing questions about the influence of army ant colony swarm‐founding and within‐colony genetic diversity on strain coexistence, and the effects of hosting a diverse suite of symbiont strains on colony ecology.

    

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4. Cophylogenetic analyses of Trachymyrmex ant‐fungal specificity: “One to one with some exceptions”

   https://doi.org/10.1111/mec.16140  

   Beigel, Katherine ; Matthews, Alix_E ; Kellner, Katrin ; Pawlik, Christine_V ; Greenwold, Matthew ; Seal, Jon_N ( September 2021 , Molecular Ecology)

   Over the past few decades, large‐scale phylogenetic analyses of fungus‐gardening ants and their symbiotic fungi have depicted strong concordance among major clades of ants and their symbiotic fungi, yet within clades, fungus sharing is widespread among unrelated ant lineages. Sharing has been explained using a diffuse coevolution model within major clades. Understanding horizontal exchange within clades has been limited by conventional genetic markers that lack both interspecific and geographic variation. To examine whether reports of horizontal exchange were indeed due to symbiont sharing or the result of employing relatively uninformative molecular markers, samples ofTrachymyrmex arizonensisandTrachymyrmex pomonaeand their fungi were collected from native populations in Arizona and genotyped using conventional marker genes and genome‐wide single nucleotide polymorphisms (SNPs). Conventional markers of the fungal symbionts generally exhibited cophylogenetic patterns that were consistent with some symbiont sharing, but most fungal clades had low support. SNP analysis, in contrast, indicated that each ant species exhibited fidelity to its own fungal subclade with only one instance of a colony growing a fungus that was otherwise associated with a different ant species. This evidence supports a pattern of codivergence betweenTrachymyrmexspecies and their fungi, and thus a diffuse coevolutionary model may not accurately predict symbiont exchange. These results suggest that fungal sharing across host species in these symbioses may be less extensive than previously thought.

    

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5. Novel insights into symbiont population structure: Globe‐trotting avian feather mites contradict the specialist–generalist variation hypothesis

   https://doi.org/10.1111/mec.17115  

   Matthews, Alix E. ; Boves, Than J. ; Sweet, Andrew D. ; Ames, Elizabeth M. ; Bulluck, Lesley P. ; Johnson, Erik I. ; Johnson, Matthew ; Lipshutz, Sara E. ; Percy, Katie L. ; Raybuck, Douglas W. ; et al ( August 2023 , Molecular Ecology)

   Researchers often examine symbiont host specificity as a species‐level pattern, but it can also be key to understanding processes occurring at the population level, which are not as well understood. The specialist–generalist variation hypothesis (SGVH) attempts to explain how host specificity influences population‐level processes, stating that single‐host symbionts (specialists) exhibit stronger population genetic structure than multi‐host symbionts (generalists) because of fewer opportunities for dispersal and more restricted gene flow between populations. However, this hypothesis has not been tested in systems with highly mobile hosts, in which population connectivity may vary temporally and spatially. To address this gap, we tested the SGVH on proctophyllodid feather mites found on migratory warblers (family Parulidae) with contrasting host specificities,Amerodectes protonotaria(a host specialist ofProtonotaria citrea) andA. ischyros(a host generalist of 17 parulid species). We used a pooled‐sequencing approach and a novel workflow to analyse genetic variants obtained from whole genome data. Both mite species exhibited fairly weak population structure overall, and contrary to predictions of the SGVH, the generalist was more strongly structured than the specialist. These results may suggest that specialists disperse more freely among conspecifics, whereas generalists sort according to geography. Furthermore, our results may reflect an unexpected period for mite transmission – during the nonbreeding season of migratory hosts – as mite population structure more closely reflects the distributions of hosts during the nonbreeding season. Our findings alter our current understanding of feather mite biology and highlight the potential for studies to explore factors driving symbiont diversification at multiple evolutionary scales.

    

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