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Abstract Evolution results from the interaction of stochastic and deterministic processes that create a web of historical contingency, shaping gene content and organismal function. To understand the scope of this interaction, we examine the relative contributions of stochasticity, determinism, and contingency in shaping gene inactivation in 34 lineages of endosymbiotic bacteria,Sodalis, found in parasitic lice,Columbicola, that are independently undergoing genome degeneration. Here we show that the process of genome degeneration in this system is largely deterministic: genes involved in amino acid biosynthesis are lost while those involved in providing B-vitamins to the host are retained. In contrast, many genes encoding redundant functions, including components of the respiratory chain and DNA repair pathways, are subject to stochastic loss, yielding historical contingencies that constrain subsequent losses. Thus, while selection results in functional convergence between symbiont lineages, stochastic mutations initiate distinct evolutionary trajectories, generating diverse gene inventories that lack the functional redundancy typically found in free-living relatives. 

Islands are well known for their unique biodiversity and significance in evolutionary and ecological studies. Nevertheless, the extinction of island species accounts for most human-caused extinctions in recent time scales, which have accelerated in recent centuries. Pigeons and doves (Columbidae) are noteworthy for the high number of island endemics, as well as for the risks those species have faced since human arrival. On Caribbean islands, no other columbid has generated more phylogenetic interest and uncertainty than the blue-headed quail-dove,Starnoenas cyanocephala. This endangered Cuban endemic has been considered more similar, both behaviourally and phenotypically, to Australasian species than to the geographically closer ‘quail-dove’ (Geotrygons.l.) species of the Western Hemisphere. Here, we use whole genome sequencing fromStarnoenasand other newly sequenced columbids in combination with sequence data from previous publications to investigate its relationships. Phylogenomic analyses, which represent 35 of the 51 genera currently comprising the Columbidae, reveal that the blue-headed quail-dove is the sole representative of a lineage diverging early in the radiation of columbids.Starnoenasis sister to the species-rich subfamily Columbinae, which is found worldwide. As a highly distinctive evolutionary lineage lacking close modern relatives, we recommend elevating the conservation priority ofStarnoenas. 

Organisms that have repeatedly evolved similar morphologies owing to the same selective pressures provide excellent cases in which to examine specific morphological changes and their relevance to the ecology and evolution of taxa. Hosts of permanent parasites act as an independent evolutionary experiment, as parasites on these hosts are thought to be undergoing similar selective pressures. Parasitic feather lice have repeatedly diversified into convergent ecomorphs in different microhabitats on their avian hosts. We quantified specific morphological characters to determine (i) which traits are associated with each ecomorph, (ii) the quantitative differences between these ecomorphs, and (iii) if there is evidence of displacement among co-occurring lice as might be expected under louse–louse competition on the host. We used nano-computed tomography scan data of 89 specimens, belonging to four repeatedly evolved ecomorphs, to examine their mandibular muscle volume, limb length and three-dimensional head shape data. Here, we find evidence that lice repeatedly evolve similar morphologies as a mechanism to escape host defences, but also diverge into different ecomorphs related to the way they escape these defences. Lice that co-occur with other genera on a host exhibit greater morphological divergence, indicating a potential role of competition in evolutionary divergence. 

Abstract The effective population size (Ne) of an organism is expected to be generally proportional to the total number of individuals in a population. In parasites, we might expect the effective population size to be proportional to host population size and host body size, because both are expected to increase the number of parasite individuals. However, among other factors, parasite populations are sometimes so extremely subdivided that high levels of inbreeding may distort these predicted relationships. Here, we used whole-genome sequence data from dove parasites (71 feather louse species of the genus Columbicola) and phylogenetic comparative methods to study the relationship between parasite effective population size and host population size and body size. We found that parasite effective population size is largely explained by host body size but not host population size. These results suggest the potential local population size (infrapopulation or deme size) is more predictive of the long-term effective population size of parasites than is the total number of potential parasite infrapopulations (i.e., host individuals). 

Next-generation sequencing technologies are revolutionizing the fields of genomics, phylogenetics, and population genetics. These new genomic approaches have been extensively applied to a major group of parasites, the lice (Insecta: Phthiraptera) of birds and mammals. Two louse genomes have been assembled and annotated to date, and these have opened up new resources for the study of louse biology. Whole genome sequencing has been used to assemble large phylogenomic datasets for lice, incorporating sequences of thousands of genes. These datasets have provided highly supported trees at all taxonomic levels, ranging from relationships among the major groups of lice to those among closely related species. Such approaches have also been applied at the population scale in lice, revealing patterns of population subdivision and inbreeding. Finally, whole genome sequence datasets can also be used for additional study beyond that of the louse nuclear genome, such as in the study of mitochondrial genome fragmentation or endosymbiont function. 

Mammals host a wide diversity of parasites. Lice, comprising more than 5,000 species, are one group of ectoparasites whose major lineages have a somewhat patchwork distribution across the major groups of mammals. Here we explored patterns in the diversification of mammalian lice by reconstructing a higher-level phylogeny of these lice, leveraging whole genome sequence reads to assemble single-copy orthologue genes across the genome. The evolutionary tree of lice indicated that three of the major lineages of placental mammal lice had a single common ancestor. Comparisons of this parasite phylogeny with that for their mammalian hosts indicated that the common ancestor of elephants, elephant shrews and hyraxes (that is, Afrotheria) was the ancestral host of this group of lice. Other groups of placental mammals obtained their lice via host-switching out of these Afrotherian ancestors. In addition, reconstructions of the ancestral host group (bird versus mammal) for all parasitic lice supported an avian ancestral host, indicating that the ancestor of Afrotheria acquired these parasites via host-switching from an ancient avian host. These results shed new light on the long-standing question of why the major groups of parasitic lice are not uniformly distributed across mammals and reveal the origins of mammalian lice. 

Abstract Host‐specialist parasites of endangered large vertebrates are in many cases more endangered than their hosts. In particular, low host population densities and reduced among‐host transmission rates are expected to lead to inbreeding within parasite infrapopulations living on single host individuals. Furthermore, spatial population structures of directly‐transmitted parasites should be concordant with those of their hosts. Using population genomic approaches, we investigated inbreeding and population structure in a host‐specialist seal louse (Echinophthirius horridus) infesting the Saimaa ringed seal (Phoca hispida saimensis), which is endemic to Lake Saimaa in Finland, and is one of the most endangered pinnipeds in the world. We conducted genome resequencing of pairs of lice collected from 18 individual Saimaa ringed seals throughout the Lake Saimaa complex. Our analyses showed high genetic similarity and inbreeding between lice inhabiting the same individual seal host, indicating low among‐host transmission rates. Across the lake, genetic differentiation among individual lice was correlated with their geographic distance, and assignment analyses revealed a marked break in the genetic variation of the lice in the middle of the lake, indicating substantial population structure. These findings indicate that movements of Saimaa ringed seals across the main breeding areas of the fragmented Lake Saimaa complex may in fact be more restricted than suggested by previous population‐genetic analyses of the seals themselves. 

Abstract The mitochondrial genomes (mitogenomes) of bilaterian animals are highly conserved structures that usually consist of a single circular chromosome. However, several species of parasitic lice (Insecta: Phthiraptera) possess fragmented mitogenomes, where the mitochondrial genes are present on separate, circular chromosomes. Nevertheless, the extent, causes, and consequences of this structural variation remain poorly understood. Here, we combined new and existing data to better understand the evolution of mitogenome fragmentation in major groups of parasitic lice. We found strong evidence that fragmented mitogenomes evolved many times within parasitic lice and that the level of fragmentation is highly variable, including examples of heteroplasmic arrangements. We also found a significant association between mitochondrial fragmentation and signatures of relaxed selection. Mitochondrial fragmentation was also associated with changes to a lower AT%, possibly due to differences in mutation biases. Together, our results provide a significant advance in understanding the process of mitogenome fragmentation and provide an important perspective on mitochondrial evolution in eukaryotes. 

Abstract Background Feather feeding lice are abundant and diverse ectoparasites that complete their entire life cycle on an avian host. The principal or sole source of nutrition for these lice is feathers. Feathers appear to lack four amino acids that the lice would require to complete development and reproduce. Several insect groups have acquired heritable and intracellular bacteria that can synthesize metabolites absent in an insect’s diet, allowing insects to feed exclusively on nutrient-poor resources. Multiple species of feather feeding lice have been shown to harbor heritable and intracellular bacteria. We expected that these bacteria augment the louse’s diet with amino acids and facilitated the evolution of these diverse and specialized parasites. Heritable symbionts of insects often have small genomes that contain a minimal set of genes needed to maintain essential cell functions and synthesize metabolites absent in the host insect’s diet. Therefore, we expected the genome of a bacterial endosymbiont in feather lice would be small, but encode pathways for biosynthesis of amino acids. Results We sequenced the genome of a bacterial symbiont from a feather feeding louse ( Columbicola wolffhuegeli ) that parasitizes the Pied Imperial Pigeon ( Ducula bicolor ) and used its genome to predict metabolism of amino acids based on the presence or absence of genes. We found that this bacterial symbiont has a small genome, similar to the genomes of heritable symbionts described in other insect groups. However, we failed to identify many of the genes that we expected would support metabolism of amino acids in the symbiont genome. We also evaluated other gene pathways and features of the highly reduced genome of this symbiotic bacterium. Conclusions Based on the data collected in this study, it does not appear that this bacterial symbiont can synthesize amino acids needed to complement the diet of a feather feeding louse. Our results raise additional questions about the biology of feather chewing lice and the roles of symbiotic bacteria in evolution of diverse avian parasites.