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Clayton, D. H.

Publications and source records attributed to Clayton, D. H..

6 recordsLinked to original sources

Independent and repeated acquisition of endosymbiotic bacteria across the diversification of feather lice

Many parasitic insects, including lice, form close relationships with endosymbiotic bacteria that are crucial for their survival. In this study, we used genomic sequencing to investigate the distribution and evolutionary history of the bacterial genus Sodalis across a broad range of feather louse species spanning 156 genera. Phylogenomic analysis revealed significant diversity among Sodalis lineages in feather lice, and robust evidence for their independent and repeated acquisition by different louse clades throughout their radiation. Among the 1,020 louse genomes analyzed, at least 22% contained Sodalis, distributed across 57 louse genera. Cophylogenetic analyses between the Sodalis and feather louse phylogenies indicated considerable mismatch. This phylogenetic incongruence between lice and Sodalis, along with the presence of distantly related Sodalis lineages in otherwise closely related louse species, strongly indicates repeated independent acquisition of this endosymbiont. Additionally, evidence of cospeciation among a few closely related louse species, coupled with frequent acquisition of these endosymbionts from free-living bacteria, further highlights the diverse evolutionary processes shaping Sodalis endosymbiosis in feather lice.

evolutionary biology↗

Genomics of experimental adaptive radiation in the cryptic coloration of feather lice

1A major challenge faced by living organisms is adaptation to novel environments. This process is poorly understood because monitoring genetic changes in natural populations is difficult. One way to simplify the task is to focus on organisms that can be studied in captivity under conditions that remain largely natural. Feather lice (Insecta, Phthiraptera, Ischnocera) are host-specific parasites of birds that live, feed, and breed solely on feathers. Birds defend themselves against lice, which damage feathers, by killing them with their beaks during bouts of preening. In response, feather lice have evolved background-matching cryptic coloration to help them avoid preening. We experimentally manipulated the color backgrounds of host-specific pigeon lice (Columbicola columbae) by confining them to different colored breeds of rock pigeon (Columba livia) over a period of four years (ca. 60 louse generations). Over the course of the experiment, we sampled lice from pigeons every six months for genomic resequencing, and then calculated allele frequency differences and trajectories to identify putative genomic sites under selection. We documented many loci that changed in response to selection for color. Most loci putatively under selection were unshared among replicate populations of lice, indicating that independent adaptation of distinct lineages to the same novel environment resulted in similar phenotypes driven by different genotypes.

evolutionary biology↗

Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites

Adaptive radiation is an important mechanism of organismal diversification, and can be triggered by new ecological opportunities. Although poorly studied in this regard, parasites present an ideal system to study adaptive radiations because of their close associations with host species. Both experimental and comparative studies suggest that the ectoparasitic wing lice of pigeons and doves have undergone an adaptive radiation, resulting in differences in both body size and overall coloration. Here we show that long-distance dispersal by dove hosts was important for parasite diversification, providing new ecological opportunities for parasites to speciate by host-switching. We further show that these new opportunities for host-switching decreased over time, and cospeciation became the more dominant mode of parasite speciation. Taken together, our results suggest that host dispersal, followed by host-switching, provided novel ecological opportunities that facilitated adaptive radiation by parasites.

evolutionary biology↗

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

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.

genomics↗

Experimental evolution of reproductive isolation from a single natural population

Ecological speciation occurs when local adaptation generates reproductive isolation as a by-product of natural selection1-3. Although ecological speciation is a fundamental source of diversification, the mechanistic link between natural selection and reproductive isolation remains poorly understood, especially in natural populations2-6. Here we show that experimental evolution of parasite body size over four years (ca. 60 generations) leads to reproductive isolation in natural populations of feather lice on birds. When lice are transferred to pigeons of different sizes they rapidly evolve differences in body size that are correlated with host size. These size differences trigger mechanical mating isolation between lice that are locally adapted to the different sized hosts. Size differences among lice also influence the outcome of competition between males for access to females. Thus, body size directly mediates reproductive isolation through its influence on both inter-sexual compatibility and intra-sexual competition. Our results confirm that divergent natural selection acting on a single phenotypic trait can cause reproductive isolation to emerge from a single natural population in real time.

evolutionary biology↗

Host defense triggers rapid adaptive radiation in experimentally evolving parasites

Adaptive radiation occurs when the members of a single lineage evolve different adaptive forms in response to selection imposed by competitors or predators. Iconic examples include Darwins finches, Caribbean anoles, and Hawaiian silverswords, all of which live on islands. Parasites, which live on host \"islands,\" show macroevolutionary patterns consistent with adaptive radiation in response to host-imposed selection. Here we show rapid adaptive divergence of experimentally evolving feather lice in response to preening, the main host defense. We demonstrate that host defense exerts strong phenotypic selection for crypsis in lice transferred to different colored rock pigeons (Columba livia). During four years of experimental evolution ([~]60 generations), the lice evolved heritable differences in color. The color differences spanned the phenotypic distribution of congeneric species of lice adapted to other species of pigeons. Our results indicate that host-mediated selection triggers rapid divergence in the adaptive radiation of parasites, which are among the most diverse organisms on earth. Our research suggests that host defense should be included with competition and predation as a major mechanism driving the evolution of biodiversity by adaptive radiation.

evolutionary biology↗