Phylogenomic analysis of seal lice reveals codivergence with their hosts

Abstract

Lice are considered a model system for studying the process of cospeciation because they are obligate and permanent parasites and are often highly host‐specific. Among lice, species in the family Echinophthiriidae Enderlein (Anoplura) are unique in that they infest mammalian hosts with an amphibious lifestyle, i.e. pinnipeds and the river otter. There is evidence that the ancestor of this group infested the terrestrial ancestor of pinnipeds, which suggests these parasites coevolved with their hosts during the transition to marine environments. However, there has been no previous study investigating the phylogenetic relationships among sucking lice parasitizing seals and sea lions. To uncover the evolutionary history of these parasites, we obtained genomic data for Antarctophthirus microchir Trouessart and Neumann (from two hosts), Antarctophthirus carlinii Leonardi et al., Antarctophthirus lobodontis Enderlein, Antarctophthirus ogmorhini Enderlein, Lepidophthirus macrorhini Enderlein, and Proechinophthirus fluctus Ferris. From genomic sequence reads, we assembled > 1000 nuclear genes and used these data to infer a phylogenetic tree for these lice. We also used the assembled genes in combination with read‐mapping to estimate heterozygosity and effective population size from individual lice. Our analysis supports the monophyly of lice from pinnipeds and uncovers phylogenetic relationships within the group. Surprisingly, we found that A. carlinii, A. lobodontis, and A. ogmorhini have very little genetic divergence among them, whereas the divergence between different geographic representatives of A. microchir indicate that they are possibly different species. Nevertheless, our phylogeny of Echinophthiriidae suggests that these lice have consistently codiverged with their hosts with minimal host switching. Population genomic metrics indicate that louse effective population size is linked to host demographics, which further highlights the close association between pinnipeds and their lice.

Patterns of Microbiome Variation Among Infrapopulations of Permanent Bloodsucking Parasites

“…The sucking lice of pinnipeds (seals, sea lions, and walrus) are of particular interest because of their need to adapt to the aquatic lifestyle of their hosts (Durden and Musser, 1994;Leonardi et al, 2013). There is evidence that the sucking lice of seals and sea lions have codiversified with their hosts (Kim, 1971(Kim, , 1975(Kim, , 1985Leonardi et al, 2019). Indeed, the sucking lice of pinnipeds represent an interesting system in which to study the variation in microbiome composition and the drivers of this variation at an intraspecific level because: (1) these lice have well defined, isolated populations (infrapopulations) on individual seal hosts, due to an expected low rate of horizontal dispersal among host individuals, which is only possible during the seals' haul-out periods on land or ice (Kim, 1985;Leonardi et al, 2013Leonardi et al, , 2019; and (2) these lice feed only upon the blood of their host (Snodgrass, 1944;Kim, 1985), so that it can be assumed that individuals from the same infrapopulation feed upon "exactly" the same resource (i.e., the blood of the individual seal on which they occur).…”

The seal louse (Echinophthirius horridus) in the Dutch Wadden Sea: investigation of vector-borne pathogens

“…Due to these morphological adaptions and a strict specifity to semiaquatic host species, a coevolution of echinophthiriid lice and their hosts has been suggested [ 13 , 18 , 19 ]. Thereby, it has been proposed that the ancestors of pinnipeds must have already been infested with ancestral sucking lice before they ventured into the marine habitat [ 8 , 20 ].…”

The seal louse (Echinophthirius horridus) in the Dutch Wadden Sea: investigation of vector-borne pathogens

“…Due to these morphological adaptions and a strict speci ty to semiaquatic host species, a coevolution of echinophthiriid lice and their hosts has been suggested [12,17,18]. Thereby, it has been proposed that the ancestors of pinnipeds must have already been infested with ancestral sucking lice before they ventured into the marine habitat [8,19].…”