Molecular phylogeny of gill monogeneans (Platyhelminthes, Monogenea, Dactylogyridae) and colonization of Indo-West Pacific butterflyfish hosts (Perciformes, Chaetodontidae)

We investigated the phylogenetic relationships among monogenean parasites of the Chaetodontidae (butterflyfishes) from the Indo-West Pacific Ocean. Molecular phylogenies of selected taxa within the Dactylogyridae, including the ancyrocephaline parasites of butterflyfishes, based on two nuclear and one mitochondrial gene fragments (complete 18S rDNA, partial 28S rDNA (D1-D3), and partial 16S rDNA) were reconstructed using parsimony, maximum likelihood and Bayesian inference methods. Our results show the non-monophyletic nature of the monogenean fauna of butterflyfishes. The group is divided into two independent lineages. The first clade contains species of the genera Aliatrema and Euryhaliotrematoides , which parasitize Chaetodontidae exclusively. The second contains species of Haliotrema , a generalist group of parasites. The positions of several other species of the Ancyrocephalinae, including freshwater species, at the base of the two clades, provide strong evidence that the monogenean fauna did not result from a single colonization event, but rather that they have colonized their butterflyfish hosts independently at least twice.     

Contrasting phylogeography of two Western Palaearctic fish parasites despite similar life cycles

Aim

We used comparative phylogeography of two intestinal parasites of freshwater fish to test whether similarity in life cycle translates into concordant phylogeographical history. The thorny‐headed worms Pomphorhynchus laevis and P. tereticollis (Acanthocephala) were formerly considered as a single species with a broad geographical and host range within the Western Palaearctic.

Location

Central and eastern parts of Northern Mediterranean area, Western and Central Europe, Ponto‐Caspian Europe.

Methods

A mitochondrial marker (COI) was sequenced for 111 P. laevis and 50 P. tereticollis individuals and nuclear ITS1 and ITS2 sequences were obtained for 37 P. laevis and 21 P. tereticollis. Genetic divergence, phylogenetic relationships and divergence time were estimated for various lineages within each species, and their phylogeographical patterns were compared to known palaeogeographical events in Western Palaearctic. Biogeographical histories of each species were inferred.

Results

The two species show very different phylogeographical patterns. Five lineages were identified in P. laevis, partially matching several major biogeographical regions defined in the European riverine fish fauna. The early stages of P. laevis diversification occurred in the peri‐Mediterranean area, during the Late Miocene. Subsequent expansion across Western Europe and Russia was shaped by dispersal and vicariant events, from Middle Pliocene to Middle Pleistocene. By contrast, P. tereticollis has differentiated more recently within the Western and Central parts of Europe, and shows weak geographical and genetic structuring.

Conclusion

Our study highlights weak to moderate similarity in the phylogeographical pattern of these acanthocephalan parasites compared to their amphipod and fish hosts. The observed differences in the timing of dispersion and migration routes taken may reflect the use of a range of final hosts with different ecologies and dispersal capabilities. By using a group underrepresented in phylogeographical studies, our study is a valuable contribution to revealing the biogeography of host–parasite interactions in continental freshwaters.     

A phylogeographical analysis across three biogeographical provinces of the south-eastern Pacific: the case of the marine gastropod Concholepas concholepas

Aim The present‐day population structure of a species reflects the influence of population history as well as contemporary processes. Little is known about the mechanisms that have shaped the geographical distribution of genetic diversity in marine species present on the south‐eastern Pacific (SEP) coast. Here we provide the first comprehensive phylogeographical study of a species distributed along the SEP coast by analysing the endemic and emblematic muricid gastropod Concholepas concholepas. Location The study localities were distributed along the SEP coast ranging from Matarani (11° S) to Puerto Eden (49° S), crossing three major biogeographical provinces: Peruvian Province, Intermediate Area and Magellanic Province. Methods A total of 337 specimens of C. concholepas were collected from 14 localities in the three biogeographical provinces/areas. Mitochondrial cytochrome oxidase I (COI) gene partial sequences (658 bp) were obtained and analysed using coalescence‐based methods to infer molecular diversity and phylogeographical patterns. Results Across the 337 individuals, we found a large diversity, with a total of 179 haplotypes at the COI gene fragment. Although a slight decrease in gene diversity was observed from north to south, an analysis of molecular variance did not reveal any significant spatial population differentiation from Peru to the tip of Chile, not even across the recognized biogeographical boundaries at 30° S and 42° S. In addition, a star‐like haplotype network suggested the past occurrence of a rapid demographic and geographical expansion over the total range examined. Calculations of the onset of this expansion suggest that it might be due to climatic conditions during the period of the marine isotope stage 11 (MIS 11, 400,000 years ago), the longer and warmer interglacial episode during the Pleistocene epoch. Main conclusions Our phylogeographical analyses indicate that in the recent past C. concholepas mitochondrial DNA lineages underwent a sudden population expansion event. In addition, our data do not support the hypothesis of concordance between biogeographical barriers and phylogeographical breaks along the SEP coast. These two results are in accordance with the paradigm of high larval dispersal ability in marine species with an extended pelagic larval phase.     

Comparative phylogeography of two seastars and their ectosymbionts within the Coral Triangle

Repeated exposure and flooding of the Sunda and Sahul shelves during Pleistocene sea‐level fluctuations is thought to have contributed to the isolation and diversification of sea‐basin populations within the Coral Triangle. This hypothesis has been tested in numerous phylogeographical studies, recovering an assortment of genetic patterns that the authors have generally attributed to differences in larval dispersal capability or adult habitat specificity. This study compares phylogeographical patterns from mitochondrial COI sequences among two co‐distributed seastars that differ in their adult habitat and dispersal ability, and two seastar ectosymbionts that differ in their degree of host specificity. Of these, only the seastar Linckia laevigata displayed a classical pattern of Indian‐Pacific divergence, but with only moderate genetic structure (Φ_CT = 0.067). In contrast, the seastar Protoreaster nodosus exhibited strong structure (Φ_CT = 0.23) between Teluk Cenderawasih and the remainder of Indonesia, a pattern of regional structure that was echoed in L. laevigata (Φ_CT = 0.03) as well as its obligate gastropod parasite Thyca crystallina (Φ_CT = 0.04). The generalist commensal shrimp, Periclimenes soror showed little genetic structuring across the Coral Triangle. Despite species‐specific phylogeographical patterns, all four species showed departures from neutrality that are consistent with massive range expansions onto the continental shelves as the sea levels rose, and that date within the Pleistocene epoch. Our results suggest that habitat differences may affect the manner in which species responded to Pleistocene sea‐level fluctuations, shaping contemporary patterns of genetic structure and diversity.     

Phylogeography of the marine isopod Stenosoma nadejda (Rezig, 1989) in North African Atlantic and western Mediterranean coasts reveals complex differentiation patterns and a new species

The transition zone between the Mediterranean and Atlantic basins has been extensively addressed in phylogeographical studies of marine species. However, biases exist towards the analysis of highly dispersive species, and there is a higher sampling effort in European coasts compared to North Africa. This may be hindering a detailed understanding of the historical and contemporary processes that shaped patterns of population genetic structure in the region. In the present study, we investigated the phylogeographical and phylogenetic patterns of mitochondrial cytochrome c oxidase subunit I sequences from a species with direct development and low dispersal abilities, Stenosoma nadejda (Rezig, 1989). The study area included 13 localities along the Atlantic and Mediterranean North African coasts, as well as the Alboran Sea. A new Stenosoma species, from the coasts of Algeria and Alboran Island, was discovered. For S. nadejda, phylogeographical analyses revealed three distinct clades: one in the Iberian Atlantic plus the Alboran Sea, one in the western Mediterranean, and another in the Atlantic coast of Africa. Haplotypes from the Alboran Island were more related to those from the western Mediterranean coast (east of the Almeria–Oran Front). Given the strong differentiation, it is probable that this species survived in multiple glacial refugia during the Pleistocenic glaciations. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 419–431.     

Spatial distribution and coexistence of monogenean gill parasites inhabiting two damselfishes from Moorea island in French Polynesia

The ectoparasite fauna of two damselfishes, Stegastes nigricans and Dascyllus aruanus, from Moorea Island in French Polynesia was investigated. Gills of these damselfishes were infected with congeneric Monopisthocotylea Monogenea belonging to the genus Haliotrema. Stegastes nigricans were found to harbour a guild of three Haliotrema species whereas only one species inhabited D. aruanus. Microhabitat distribution, inter- and intraspecific competition and interspecific associations on the gill were studied. Observations on site preference revealed no spatial segregation between the three congeneric species inhabiting the gills of S. nigricans. Juvenile and adult monogeneans of that guild occurred on the same microhabitat. The dominant species Haliotrema sp. 1 did not expand on the microhabitat when the intensity of infection increased. Interspecific association tests revealed positive and negative associations. Haliotrema sp. 4 expanded its distribution on the gills of Dascyllus aruanus when the intensity of infection increased suggesting the likelihood of intraspecific competition. Juvenile and adult monogeneans of Haliotrema sp. 4 appeared to segregate as a result of intraspecific competition. This competition may exist to enhance resource availability when the gill habitat is limited. Overlaps between niche breadth and species microhabitat were revealed for monogenean species inhabiting S. nigricans. Interspecific competition did not appear to play an important role in the distribution of S. nigricans congeneric ectoparasites. Reinforcement of reproductive barriers may have led to the avoidance of hybridization.     

Forest refugia and riverine barriers promote diversification in the West African pygmy shrew (Crocidura obscurior complex,Soricomorpha)

The Crocidura obscurior or West African pygmy shrew complex is endemic to West African forests from south‐eastern Guinea, eastern Liberia, southern Côte d'Ivoire and south‐western Ghana. We explore the genetic and morphometric diversity of 239 individuals of the C. obscurior complex from 17 localities across its geographical range. Using genetic data from three mitochondrial (16S, cytochrome b and COI) and four nuclear markers (BRCA1, STAT5A, HDAC2 and RIOK3) and skull geometric morphometrics, we show that this complex is composed of two cryptic and sympatric species, C. obscurior and C. eburnea. We then test several hypotheses to infer their evolutionary history. The observed phylogeographical pattern based on cytochrome b and COI sequences fits the forest refuge theory: during arid phases of the Plio‐Pleistocene, around 3.5, 2.1, 1 and 0.5 Mya, a small number of populations survived in isolated forest patches and diverged allopatrically. During wetter climatic periods, forests expanded, leading to secondary contacts between previously isolated populations. Our results also suggest the possible contribution of episodes of isolation in subrefuges. Historical variation of the West African hydrographic network could also have contributed to the observed patterns of genetic differentiation. Rivers such as the Volta and Sassandra may act as past and/or current barriers to gene flow. Although these two species have sympatric distributions, their phylogeographical histories are somewhat dissimilar due to small differences in their dispersal abilities and ecological requirements.     

Phylogeographical pattern of Mazocraeoides gonialosae (Monogenea, Mazocraeidae) on the dotted gizzard shad, Konosirus punctatus, along the coast of China

In the present study, we examined the phylogeographical pattern of the monogenean, Mazocraeoides gonialosae, which parasitises the dotted gizzard shad (Konosirus punctatus) along the coast of China. Fragments of 756 bp of the mitochondrial cytochrome c oxidase subunit I gene were sequenced for 147 individuals from seven localities along the coast of China. Phylogenetic analysis revealed no significant genealogical clades of samples corresponding to sampling localities. Analyses of molecular variance and pairwise F_ST suggested a high rate of gene flow and the lack of a predictable genetic structure between different populations of this parasite. Both neutrality tests and mismatch distribution analyses indicated a recent population expansion in M. gonialosae after the last glacial maximum. Gradually decreasing genetic diversity in more northerly populations implied a historical south-to-north expansion of this parasite. Dispersal of eggs and larvae with ocean currents was considered to be associated with the genetic homogeneity of this species. The limited time to accumulate genetic variation after the last glacial maximum may also account in part for the lack of phylogeographical structure in the studied region.     

Mites as biological tags of their hosts

Movements and spatial distribution of host populations are expected to shape the genetic structure of their parasite populations. Comparing the genetic patterns of both interacting species may improve our understanding of their evolutionary history. Moreover, genetic analyses of parasites with horizontal transmission may serve as indicators of historical events or current demographic processes that are not apparent in the genetic signature of their hosts. Here, we compared mitochondrial variation in populations of the ectoparasitic mite Spinturnix myoti with the genetic pattern of its host, the Maghrebian bat Myotis punicus in North Africa and in the islands of Corsica and Sardinia. Mite mitochondrial differentiation among populations was correlated with both host mitochondrial and nuclear differentiation, suggesting spatial co‐differentiation of the lineages of the two interacting species. Therefore our results suggest that parasite dispersal is exclusively mediated by host movements, with open water between landmasses as a main barrier for host and parasite dispersal. Surprisingly the unique presence of a continental European mite lineage in Corsica was inconsistent with host phylogeographical history and strongly suggests the former presence of European mouse‐eared bats on this island. Parasites may thus act as biological tags to reveal the presence of their now locally extinct host.     

A link between host dispersal and parasite diversity in two sympatric cichlids of Lake Tanganyika

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The spatial distribution does not affect host–parasite coevolution in <Emphasis Type="Italic">Rossomyrmex</Emphasis> ants

Host and parasite distributions are crucial to understand the coevolutionary outcomes of their relationships. This comes from the fact that the distribution of a species (fragmented vs. continuous habitats) influences its dispersal opportunities. In this work, we studied the effect of the spatial distribution on dispersal and coevolution between three species of social parasite ants of the genus Rossomyrmex (one distributed in high mountains in Spain and two distributed in extended plains in Turkey and Kazakhstan) and their ant hosts Proformica. We analysed the variation at the mitochondrial gene cytochrome c oxidase (COI) to infer female dispersal for parasites as well as the cuticular hydrocarbons (CHCs) of parasites and hosts to study their coevolutionary process, given that CHCs are involved in nestmate recognition. Our genetic results revealed a surprising scarce variation at COI for the three parasite species, suggesting selective forces that prevent from mutation fixation. Therefore, COI appeared to be a poor tool to study dispersal. Furthermore, chemical results showed population differentiation for all host–parasite systems, pointing that coevolution would take place at a local scale regardless of the spatial distribution or dispersal opportunities of the counterparts.     

Biogeographic patterns of metazoan parasites of the bigeye flounder, Hippoglossina macrops, in the southeastern Pacific coast

We examined the metazoan parasite fauna of the bigeye flounder, Hippoglossina macrops, in a latitudinal gradient of the southeastern Pacific (ca. 25 degrees S-33 degrees S) to assess whether their parasites show latitudinal and/or biogeographical patterns, and to determine if these patterns agree well with those observed for free-living organisms. In total, 331 fish from 6 localities were analyzed. Eighteen parasite species, including 5 ecto- and 13 endoparasites, were found in the bigeye flounder. Neoheterobothrium chilensis, Floridosentis sp., and Corynosoma australe were the most prevalent parasite species. Ecto- and endoparasites of H. macrops showed different latitudinal patterns. Only endoparasite species show a distributional pattern concordant with biogeographic areas recognized for free-living organisms; this finding was supported by cluster analyses showing 2 major divisions. The first joined the most northern localities (25 degrees S-26 degrees S), and the second consisted of 2 subgroups: (1) 28 degrees S-30 degrees S, and (2) 31 degrees S-32 degrees S. A multivariate analysis of infracommunities showed significant differences in the parasitic load of H. macrops from different latitudes. The latitudinal differences in the prevalence and abundance of the parasites might be explained by differing oceanographic conditions in water masses. These physical conditions could affect the dispersal ability of the infective stages of ecto-parasites, and produce zoogeographical breaks that could affect the distribution of intermediate hosts (invertebrate and vertebrate prey), subsequently affecting the transmission of endoparasites.     

Phylogeography of a mite,Halozetes fulvus,reflects the landscape history of a young volcanic island in the sub‐Antarctic

Previous studies of the microarthropods of Marion Island, Southern Ocean, documented high mitochondrial COI (cytochrome c oxidase subunit I) haplotype diversity and significant genetic structure, which were ascribed to landscape subdivision. In this paper we revisit these ideas in light of new geomorphological evidence indicating a major lineament orientated along N26.5°E. Using the microarthropod Halozetes fulvus, we test the hypothesis that the eastern and western sides of the island show different population genetic patterns, corresponding to the previously unrecognized geological separation of these regions, and perhaps also with differences in climates across the island and further landscape complexity. Mitochondrial COI data were collected for 291 H. fulvus individuals from 30 localities across the island. Notwithstanding our sampling effort, haplotype diversity was under‐sampled as indicated by rarefaction analyses. Overall, significant genetic structure was found across the island as indicated by Φ_ST analyses. Nested clade phylogeographical analyses suggested that restricted gene flow (with isolation‐by‐distance) played a role in shaping current genetic patterns, as confirmed by Mantel tests. At the local scale, coalescent modelling revealed two different genetic patterns. The first, characterizing populations on the south‐western corner of the island, was that of low effective population size and high gene flow. The converse was found on the eastern side of Marion Island. Taken together, substantial differences in spatial genetic structure characterize H. fulvus populations across Marion Island, in keeping with the hypothesis that the complex history of the island, including the N26.5°E geological lineament, has influenced population genetic structure. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 131–145.     

Comparative phylogeography of a vulnerable bat and its ectoparasite reveals dispersal of a non-mobile parasite among distinct evolutionarily significant units of the host

Knowledge about phylogeographical structuring and genetic diversity is of key importance for the conservation of endangered species. Comparative phylogeography of a host and its parasite has the potential to reveal cryptic dispersal and behaviour in both species, and can thus be used to guide conservation management. In this study, we investigate the phylogeographic structure of the Bechstein’s bat, Myotis bechsteinii, and its ectoparasitic bat fly, Basilia nana, at 12 sites across their entire distribution. For both species, a mitochondrial sequence fragment (ND1 and COI respectively) and nuclear microsatellite genotypes (14 and 10 loci respectively) were generated and used to compare the phylogeography of host and parasite. Our findings confirm the presence of three distinct genetic subpopulations of the Bechstein’s bat in (1) Europe, (2) the Caucasus and (3) Iran, which remain isolated from one another. The genetic distinctiveness of host populations in the Caucasus region and Iran emphasize that these populations must be managed as distinct evolutionarily significant units. This phylogeographical pattern is however not reflected in its parasite, B. nana, which shows evidence for more recent dispersal between host subpopulations. The discordant genetic pattern between host and parasite suggest that despite the long-term genetic isolation of the different host subpopulations, long-range dispersal of the parasite has occurred more recently, either as the result of secondary contact in the primary host or via secondary host species. This indicates that a novel pathogenic threat to one host subpopulation may be able to disperse, and thus have important consequences for all subpopulations.     

Redescriptions of two species of microcotylid monogeneans from three arripid hosts in southern Australian waters

Microcotyle arripis Sandars, 1945 is redescribed from Arripis georgianus from four localities: Spencer Gulf, Gulf St. Vincent, off Kangaroo Island and Coffin Bay, South Australia, Australia. Kahawaia truttae (Dillon & Hargis, 1965) Lebedev, 1969 is reported from A. trutta off Bermagui, New South Wales and is redescribed from a new host, A. truttaceus, from four localities in South Australian waters: Spencer Gulf, Gulf St. Vincent, off Kangaroo Island and Coffin Bay. Phylogenetic analysis of the partial 28S ribosomal RNA gene (28S rRNA) nucleotide sequences for both microcotylid species and comparison with other available sequence data for microcotylid species across four genera contributes to our understanding of relationships in this monogenean family.     

Temperature and development in host-parasite relationships

Summary The effects of temperature on growth and development of the cabbage butterfly, Pieris rapae, and three wasp parasites: Apanteles rubecula, Apanteles glomeratus and Pteromalus puparum in Vancouver, Canada, and Canberra, Australia, are examined. We compare the estimates of temperature threshold for development and the number of degree-days above this threshold required to complete development for the immature stages of all species in both localities. Developmental patterns of both the host and its parasites differ between localities. Within the range of temperatures likely to be experienced during the host's breeding season, Australian parasites have longer generation times than their host at low temperatures and shorter generation times at high temperatures. Canadian parasites have shorter generation times, relative to the host, at all temperatures. This may be necessitated by the shorter breeding season available to the Canadian parasites.Besides temperature, parasite development is affected by host size and, in the gregarious species, parasite density. Host larval development is retarded by both Apanteles.All parasites are smaller at higher temperatures and males are smaller than females, but size is also affected by host size and parasite density.Although parasite size, and consequently fecundity, varies greatly, parasites experiencing similar temperatures will have closely similar developmental periods. The ecological significance of these developmental responses is discussed.     

Mating rendezvous in monogenean gill parasites of the humbug Dascyllus aruanus (Pisces: Pomacentridae)

The gills of the humbug, Dascyllus aruanus (Pomacentridae), were infected by a monogenean genus Haliotrema at a high prevalence (83%) but with a low mean intensity (5.6 worms/fish). All the gill arches of 365 fish, caught on the fringing reef of Moorea Island (French Polynesia), were examined for parasites. Each hemibranch was divided into 12 subequal sections. Monogeneans showing microhabitat overlap were defined as couples. Hosts with low intensity of infection (fewer than 5 monogeneans per gill) were selected and couples were recorded. Among the 37 hosts harboring 2 worms on their gills, 18 fish were infected with these 2 monogeneans on the same gill side of the body; 50% (n = 9) of these harbored monogeneans within the same gill arch and 55% (n = 5) of these last fish showed individual parasites within the same section of the gill. In the case of hosts with few monogeneans (3 and 4 individuals; n = 37) on the same arch, more than 40% (n = 16) harbored worms in couples. There may be some chemical communication that allowed these monogeneans to migrate toward each other and thus enhance mating success. Mating rendezvous appears to be a more important factor than site location for these gill monogeneans.     

Algal Parasite Herpodiscus durvillaeae (Phaeophyceae: Sphacelariales) Inferred to have Traversed the Pacific Ocean with its Buoyant Host

The parasitic phaeophycean endophyte Herpodiscus durvillaeae (Lindauer) G. R. South has previously only been recorded from New Zealand, in association with a single host species, Durvillaea antarctica (Chamisso) Hariot (southern bull‐kelp). Here we use DNA sequence data from plastid and nuclear markers (chloroplast rbcL, ribosomal LSU, and a nuclear pseudogene copy of COI) to test for the presence of H. durvillaeae beyond the New Zealand region, and on host species other than D. antarctica. Analyses of samples from the Falkland Islands confirm the first record of H. durvillaeae from the Atlantic Ocean. We report that Falkland Islands H. durvillaeae are genetically indistinguishable from samples of this species from New Zealand's sub‐Antarctic Campbell Island, suggesting recent dispersal of the parasite across the Pacific Ocean, presumably by rafting with its buoyant macroalgal host. We also here record H. durvillaeae from New Zealand endemics Durvillaea poha Fraser et al. and D. willana Lindauer.     

Comparative phylogeography of codistributed aquatic insects in western North America: insights into dispersal and regional patterns of genetic structure

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