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A newly discovered radiation of endoparasitic gastropods and their coevolution with asteroid hosts in Antarctica.
Layton KKS
,
Rouse GW
,
Wilson NG
.
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BACKGROUND: Marine invertebrates are abundant and diverse on the continental shelf in Antarctica, but little is known about their parasitic counterparts. Endoparasites are especially understudied because they often possess highly modified body plans that pose problems for their identification. Asterophila, a genus of endoparasitic gastropod in the family Eulimidae, forms cysts in the arms and central discs of asteroid sea stars. There are currently four known species in this genus, one of which has been described from the Antarctic Peninsula (A. perknasteri). This study employs molecular and morphological data to investigate the diversity of Asterophila in Antarctica and explore cophylogenetic patterns between host and parasite.
RESULTS: A maximum-likelihood phylogeny of Asterophila and subsequent species-delimitation analysis uncovered nine well-supported putative species, eight of which are new to science. Most Asterophila species were found on a single host species, but four species were found on multiple hosts from one or two closely related genera, showing phylogenetic conservatism of host use. Both distance-based and event-based cophylogenetic analyses uncovered a strong signal of coevolution in this system, but most associations were explained by non-cospeciation events.
DISCUSSION: The prevalence of duplication and host-switching events in Asterophila and its asteroid hosts suggests that synchronous evolution may be rare even in obligate endoparasitic systems. The apparent restricted distribution of Asterophila from around the Scotia Arc may be an artefact of concentrated sampling in the area and a low obvious prevalence of infection. Given the richness of parasites on a global scale, their role in promoting host diversification, and the threat of their loss through coextinction, future work should continue to investigate parasite diversity and coevolution in vulnerable ecosystems.
Fig. 1. Asterophila distribution in Antarctica. a Host specimens infected by Asterophila (left: P00407, right: P00340)- white circles indicate cysts on the asteroid arm. b
Asterophila specimens retrieved from hosts (left: M13618, right: M12882). c Localities marked with a square denote locations where Asterophila was present, and localities marked with a circle represent locations where hosts were sampled but Asterophila was absent (Wikimedia Commons contributors). d Detailed sampling map showing co-distribution of Asterophila species at South Shetland Islands created with the R package ggplot2 [27] and with bathymetry data from the National Oceanic and Atmospheric Administration (NOAA) in the R package marmap [28]
Fig. 2. Secondary species hypothesis. ML phylogeny (COI + 16S + H3 + 28S + ANT) of Asterophila representing the secondary species hypothesis, with host order-level taxonomy provided in red. Nodes with less than 50% bootstrap support have been collapsed, and triangles represent single clades. Hash marks denote that the branch has been truncated to one quarter of its original length. For species-delimitation analysis (ABGD and bPTP) black boxes represent congruent clades, red boxes represent splits within a clade, and blue boxes represent merged clades
Fig. 3. Asterophila larvae. Larval morphologies of a
Asterophila japonica, A. rathbunasteri and A. perknasteri from the literature (adapted from [15, 16] with permission) and b
A. sp. 3, A. sp. 5 and A. perknasteri from this study, with scale bar
Fig. 4. Host use by Asterophila. a ML phylogeny (COI + 16S + H3 + 28S + ANT) of Asterophila with host species designations. Nodes with less than 50% bootstrap support have been collapsed, and triangles represent single clades. Hash marks denote that the branch has been truncated to one quarter of its original length. Asterophila species in bold have been recovered from multiple host species. b Corresponding TCS haplotype networks (COI) for Asterophila species recovered from multiple hosts. Hash marks on the haplotype network correspond to mutational steps and circle size represents the number of sequences per haplotype. Colours in the haplotype network correspond to different host species
Fig. 5. Host-parasite associations. Cophylo plot of 57 host-parasite relationships between Asterophila and asteroid hosts. Branches and associations are coloured based on host order. Host colours match ancestral state reconstruction in Additional file 2: Figure S2
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