Rapid experimental evolution of reproductive isolation from a single natural population

Villa, Scott M.; Altuna, Juan C.; Ruff, James S.; Beach, Andrew B.; Mulvey, Lane I.; Poole, Erik J.; Campbell, Heidi E.; Johnson, Kevin P.; Shapiro, Michael D.; Bush, Sarah E.; Clayton, Dale H.

doi:10.1073/pnas.1901247116

Cited by 47 publications

(45 citation statements)

References 77 publications

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“…This variation makes it possible to transfer C. columbae among diverse size and color phenotypes within the single native host species. Recently, we showed that switching lice to pigeons of different sizes and colors elicits rapid population-level changes in louse size and color ( Bush et al 2019 ; Villa et al 2019 ). Despite the wealth of phenotypic data about real-time adaptation of C. columbae to changes in host environment, the underlying molecular mechanisms remain unknown.…”

Section: Introductionmentioning

confidence: 99%

The assembled and annotated genome of the pigeon louseColumbicola columbae, a model ectoparasite

Baldwin-Brown

Villa

Vickrey

et al. 2021

G3 Genes|Genomes|Genetics

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The pigeon louse Columbicola columbae is a longstanding and important model for studies of ectoparasitism and host-parasite coevolution. However, a deeper understanding of its evolution and capacity for rapid adaptation is limited by a lack of genomic resources. Here, we present a high-quality draft assembly of the C. columbae genome, produced using a combination of Oxford Nanopore, Illumina, and Hi-C technologies. The final assembly is 208 Mb in length, with 12 chromosome-size scaffolds representing 98.1% of the assembly. For gene model prediction, we used a novel clustering method (wavy_choose) for Oxford Nanopore RNA-seq reads to feed into the MAKER annotation pipeline. High recovery of conserved single-copy orthologs (BUSCOs) suggests that our assembly and annotation are both highly complete and highly accurate. Consistent with the results of the only other assembled louse genome, Pediculus humanus, we find that C. columbae has a relatively low density of repetitive elements, the majority of which are DNA transposons. Also similar to P. humanus, we find a reduced number of genes encoding opsins, G protein-coupled receptors, odorant receptors, insulin signaling pathway components, and detoxification proteins in the C. columbae genome, relative to other insects. We propose that such losses might characterize the genomes of obligate, permanent ectoparasites with predictable habitats, limited foraging complexity, and simple dietary regimes. The sequencing and analysis for this genome were relatively low-cost, and took advantage of a new clustering technique for Oxford Nanopore RNAseq reads that will be useful to future genome projects.

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Section: Introductionmentioning

confidence: 99%

The assembled and annotated genome of the pigeon louseColumbicola columbae, a model ectoparasite

Baldwin-Brown

Villa

Vickrey

et al. 2021

G3 Genes|Genomes|Genetics

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“…Our goal is to design and synthesize a new Mimulus species (sensu Duffy et al, 2007;Villa et al, 2019), pollinated by hawkmoths and reproductively isolated from its red-flowered, hummingbird-pollinated ancestor, M. cardinalis. Several traits already present in Mimulus, including nocturnal anthesis, large nectar volume in M. cardinalis, and floral scent, suggest that the evolution of hawkmoth pollination in section Erythranthe should be genetically tractable and require few mutational changes.…”

Section: Introductionmentioning

confidence: 99%

Rational Design of a Novel Hawkmoth Pollinator Interaction in Mimulus Section Erythranthe

Byers

Bradshaw

2021

Front. Ecol. Evol.

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Diversification of the ca. 275,000 extant flowering plant species has been driven in large part by coevolution with animal pollinators. A recurring pattern of pollinator shifts from hummingbird to hawkmoth pollination has characterized plant speciation in many western North American plant taxa, but in the genus Mimulus (monkeyflowers) section Erythranthe the evolution of hawkmoth pollination from hummingbird-pollinated ancestors has not occurred. We manipulated two flower color loci and tested the attractiveness of the resulting four color phenotypes (red, yellow, pink, and white) to naïve hawkmoths (Manduca sexta). Hawkmoths strongly prefer derived colors (yellow, pink, white) over the ancestral red when choosing an initial flower to visit, and generally preferred derived colors when total visits and total visit time were considered, with no hawkmoth preferring ancestral red over derived colors. The simple flower color genetics underlying this innate pollinator preference suggests a potential path for speciation into an unfilled hawkmoth-pollinated niche in Mimulus section Erythranthe, and the deliberate design of a hawkmoth-pollinated flower demonstrates a new, predictive method for studying pollination syndrome evolution.

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“…Experimental research has shown this to occur in wing lice from pigeons; lice transferred to different-sized pigeons were often unable to avoid preening behavior and were quickly removed by the host (Bush & Clayton, 2007;. This can lead to reproductive isolation between populations of lice and ultimately to speciation (Villa et al, 2019). However, host body size is likely not a crucial factor for grouse and their lice.…”

Section: Factors Influencing the Relationships Between Grouse And Tmentioning

confidence: 99%

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

Sweet

Wilson

Sonsthagen

et al. 2020

Ecology and Evolution

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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 wholegenome 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.

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Rapid experimental evolution of reproductive isolation from a single natural population

Cited by 47 publications

References 77 publications

The assembled and annotated genome of the pigeon louseColumbicola columbae, a model ectoparasite

The assembled and annotated genome of the pigeon louseColumbicola columbae, a model ectoparasite

Rational Design of a Novel Hawkmoth Pollinator Interaction in Mimulus Section Erythranthe

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

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