Reintroduction of Profilicollis Meyer, 1931, as a genus in acenthocephala: significance of the intermediate host.

Polymorphid acanthocephalans with long necks, spheroid proboscides, and eggs without polar swellings of the fertilization membrane constitute a morphologically distinct group of species. In the past, this taxon was considered a separate genus, Profilicollis. More recently, workers have been unwilling to accept these features as generic-level characters, and presently the group is considered a subgenus of Polymorphus. An analysis prompted by our studies of various polymorphid cystacanths in crabs along the coasts of Scotland and the U.S.A. reveals that all records of Polymorphus in decapods refer to species with 6 cement glands frequently assigned to Hexaglandula, to incidental occurrences of species purported to be Polymorphus minutus, or to species of the subgenus Profilicollis. Occurrence in decapod crustaceans implies substantial life history differences from the other species of the genus occurring in amphipod crustaceans. We conclude this, together with morphological distinctiveness, justifies return of Profilicollis to full generic status within Polymorphidae.     

Status of Corynosoma (Acanthocephala: Polymorphidae) based on anatomical, ecological, and phylogenetic evidence, with the erection of Pseudocorynosoma n. gen

The possession of genital spines has been considered as a key taxonomic trait to differentiate Corynosoma from other genera of the Polymorphidae. However, Corynosoma currently consists of 2 groups of species with clear ecological and morphological divergences: the "marine" group (with ca. 30 species) infects mammals and piscivorous birds in the marine realm, whereas the "freshwater" group (with ca. 7 species) infects waterfowl in continental waters. Species from these groups differ in shape of body and neck, trunk spination, lemnisci length and shape, testes arrangement, and number and shape of cement glands. We tested whether species from these 2 groups formed a monophyletic assemblage based on a phylogenetic analysis by using 15 morphological characters. We also included species of Andracantha, Polymorphus, and Hexaglandula with which potential taxonomic conflicts could most likely arise. We obtained 108 equally most parsimonious trees of 32 steps, with a consistency index (CI) = 0.59, and a retention index (RI) = 0.82. The strict consensus tree indicated that the "freshwater" species of Corynosoma form a monophyletic assemblage closely related to some species of Polymorphus, whereas the "marine" species of Corynosoma are grouped together with Andracantha. Accordingly, Corynosoma is not a monophyletic assemblage, and Pseudocorynosoma n. gen. is proposed for the "freshwater" species of Corynosoma. This decision was strongly supported by (1) a functional comparison of foretrunk muscles between species of Polymophus, Andracantha, and Corynosoma; (2) a multivariate morphometric study of proboscis characters and egg size; and (3) an analysis of ecological patterns of host-parasite relationships.     

Erection of Ibirhynchus gen. nov. (Acanthocephala: Polymorphidae), based on molecular and morphological data

The genus Southwellina is composed of 3 described species, i.e., S. hispida (the type species), S. dimorpha, and S. macracanthus. All 3 are endoparasites of fish-eating birds that have worldwide distributions. Morphologically, the genus is characterized by possessing a short and compact trunk, 2 fields of spines in the anterior region of the trunk (in at least 1 sex), a short cylindrical proboscis (sometimes with a swollen region armed with numerous longitudinal rows of hooks), a double-walled proboscis receptacle, and 4 tubular cement glands in males. In the current study, specimens identified as S. dimorpha were collected from Eudocimus albus (white ibis), the type host from the Gulf of Mexico. Sequences of 2 nuclear genes (small subunit [SSU] and long subunit [LSU] ribosomal DNA) and 1 mitochondrial gene (cytochrome c oxidase subunit 1 [cox 1]) of S. dimorpha and S. hispida were obtained and used to reconstruct the phylogenetic relationships of both species with respect to published sequences of 11 species representing 6 genera of Polymorphidae. Maximum parsimony (MP) and maximum likelihood (ML) analyses of the concatenated data set (SSU + LSU + cox 1) were identical in depicting Southwellina as paraphyletic, indicating that the genus should be revised. The MP and ML trees identified S. hispida as a sister to Polymorphus brevis, whereas S. dimorpha was a sister to Hexaglandula corynosoma. Morphologically, S. dimorpha is distinct from H. corynosoma, which is characterized by a short trunk with 1 field of spines in the anterior part of the trunk in both genders, and males with 6 tubular cement glands. The genetic divergence estimated from a concatenated data set between 2 isolates of S. hispida and S. dimorpha ranged from 10.7 to 11.0%. This range of genetic divergence is similar to that found among other genera of Polymorphidae, which extends from 6.0 to 12.0%. Southwellina dimorpha differs from S. hispida in the shape of the proboscis and the presence of 1 field of spines (S. dimorpha) versus 2 fields (S. hispida) on the anterior region of the trunk in females. Based on the phylogenetic position of S. dimorpha within Polymorphidae, coupled with levels of genetic divergence and, more importantly, the morphological and ecological (host specificity) differences, we propose the erection of a new genus to accommodate S. dimorpha.     

Polymorphus arctocephali Smales, 1986, a synonym of Corynosoma cetaceum Johnston & Best, 1942 (Acanthocephala: Polymorphidae)

Polymorphus arctocephali (Acanthocephala: Polymorphidae) was differentiated from P. cetaceum based on patterns in the trunk spine distribution and slight morphometric differences. The comparison of both species involved samples from South Australia and did not include P. cetaceum from South America. In this paper we re-examine the systematic position of P. arctocephali based on a more detailed morphological and geographical analysis. Results indicate that P. arctocephali does not differ in trunk spine distribution with respect to P. cetaceum, and that its morphometric differences can be subsumed under the natural variation found within P. cetaceum populations. Therefore, P. arctocephali becomes a junior synonym of P. cetaceum. P. cetaceum was transferred from Corynosoma to Polymorphus due to the absence of genital spines in both sexes. However, adopting the less restrictive definition of genital spines used by several authors, females of P. cetaceum could be considered as bearing genital spines. Species of the genus Andracantha also have genital spines, but specimens of P. cetaceum possess a continuous field of trunk spines, which precludes the assignment of this species to Andracantha. Other generic level characters, as well as ecological data, support clearly the transference of P. cetaceum back to Corynosoma. Therefore, this species becomes Corynosoma cetaceum Johnston & Best, 1942.     

Systematic position of Pseudocorynosoma and Andracantha (Acanthocephala, Polymorphidae) based on nuclear and mitochondrial gene sequences

Species of Pseudocorynosoma are North and South American acanthocephalans that use waterfowl as definitive hosts and amphipods as intermediate hosts, whereas species of Andracantha occur in fish-eating birds with a worldwide distribution. Pseudocorynosoma and Andracantha were originally described as Corynosoma (now restricted to endoparasites of marine mammals). Morphologically, Andracantha is distinct from other genera of Polymorphidae in possessing 2 fields of spines on the trunk, whereas Corynosoma and Pseudocorynosoma have a single field. A recent phylogenetic hypothesis based on morphological characters suggested that Andracantha is closely related to Corynosoma, whereas Pseudocorynosoma was of uncertain phylogenetic position within the Polymorphidae. To test the systematic affinities of these 3 genera, we sequenced 2 nuclear genes (SSU and LSU ribosomal DNA) and 1 mitochondrial gene (cytochrome c oxidase subunit 1; cox 1) of species representing Corynosoma, Andracantha, and Pseudocorynosoma and analyzed the data, including available sequences of other polymorphids. Maximum parsimony (MP), maximum likelihood (ML), and Bayesian analyses of the combined (SSU + LSU) sequences and the concatenated data of 3 genes (SSU + LSU + cox 1) placed Andracantha as the sister taxon to Corynosoma with robust support values. All analyses also showed that Pseudocorynosoma is an independent lineage that does not share a common ancestry with Andracantha and Corynosoma. These phylogenetic hypotheses suggest that birds were the ancestral hosts of polymorphids and that the association of Corynosoma with marine mammals represents a subsequent episode of colonization.     

Acanthocephalans from crabs in the southeastern U.S., with the first intermediate hosts known for Arhythmorhynchus frassoni and Hexaglandula corynosoma

Cystacanths of Hexaglandula corynosoma were discovered in the fiddler crabs Uca spinicarpa and Uca rapax collected in Mississippi and Florida. Adults were present in yellow-crowned night herons, Nyctanassa violacea, collected in Florida. Cystacanths are very similar to adults, varying only in size and state of development. This is the first record of H. corynosoma from the United States and the first record of an intermediate host for any species of the genus. Cystacanths of Arhythmorhynchus frassoni were present in U. rapax from Florida. The proboscis size, shape, and armature of the cystacanths are identical to those of adults from clapper rails (Rallus longirostris) collected in several southeastern states. This is the first report of an intermediate host for A. frassoni. Profilicollis altmani cystacanths were collected from mole crabs (Emerita talpoida) at Atlantic Beach, North Carolina. These specimens, together with adults obtained from shore birds in Louisiana and Mississippi, are consistent with the view that P. altmani, Profilicollis kenti, and Profilicollis texensis are synonyms, with P. altmani having nomenclatural priority.     

On a new acanthocephalan family and a new order, from birds in Vietnam

During November 2000, a collection of acanthocephalans from birds in Quang Ninh Province, Vietnam, included a new genus and species in a new family and order. Pyrirhynchus heterospinus n. gen., n. sp. (Pyrirhynchidae n. fam.: Heteramorphida: new order) is described from Actitis hypoleucos (Linnaeus, 1758) (common sandpiper). The new family combines characters from Polymorphidae and Heteracanthocephalidae, and it includes new features. Specimens of the new species are distinguished from those of Heteracanthocephalidae and/or Polymorphidae by their long cylindrical trunk with anterior swelling, pyriform proboscis with hooks much larger ventrally, brain at the anterior end of the receptacle, specialized tubular cement glands, and elliptoid eggs with concentric shells. A detailed analysis of proboscis and trunk armature is included, and specimens of several species of Arhythmorhynchus Lühe, 1911 (Polymorphidae) were studied for comparative purposes. The proboscis of P. heterospinus is armed with 17 to 20 rows of 17 to 19 hooks each, with anterior 9-11 hooks rooted and posterior 6-10 spines rootless.     

Description and host relationships of Polymorphus spindlatus n. sp. (Acanthocephala: Polymorphidae) from the heron Nycticorax nycticorax in Peru

Polymorphus spindlatus n. sp. is described from the black-crowned night heron, Nycticorax nycticorax, in Lake Titicaca, Peru. It is distinguished from all 27 known species of the subgenus Polymorphus by its spindle-shaped proboscis and its trunk shape, the anterior 2/3 of which is ovoid, tapering into a tubular posterior end. It resembles Polymorphus brevis (=Arhythmorhynchus brevis), which is, however, longer and considerably more slender, and has smaller and more numerous proboscis hooks per row and smaller eggs. It is separated also from Polymorphus swartzi, Polymorphus striatus, Polymorphus contortus, and Polymorphus cincli by its proboscis armature (usually 18 longitudinal rows of 11-13 hooks each), among other characters. Histopathological sections of host tissue show well defined localized damage including hemorrhaging with subsequent phagocyte cell migration (granular tissue). The lumen of the host intestine is obstructed and villi show compression. The proboscis of P. spindlatus extends through the intestinal mucosa and submucosa, displacing the smooth muscle layers of the muscularis externa. Fibrosis also was observed.     

The Peculiarities of Parasiting of Polymorphus phippsi (Palaeacanthocephala: Polymorphidae) in the Intestines of Seabirds from the Barents Sea

Biology Bulletin - Aspects of the localization and digestion physiology of the acanthocephalan Polymorphus phippsi (Kostylew, 1922) (Palaeacanthocephala: Polymorphidae) from the intestines of...     

Profilicollis novaezelandensis n. sp. (Polymorphidae) and two other acanthocephalan parasites from shore birds (Haematopodidae and Scolopacidae) in New Zealand,with records of two species in intertidal crabs (Decapoda: Grapsidae and Ocypodidae)

Profilicollis novaezelandensis n. sp. (Acanthocephala: Polymorphidae) is described from the South Island pied oystercatcher Haematopus ostralegus finschi Martens (Haematopodidae) and the intertidal crab Hemigrapsus crenulatus (Milne Edwards) (Brachyura: Grapsidae) from the South Island of New Zealand. The new species can be distinguished from all the other species of the genus by a combination of the following characters: long neck (13% of total body length for adults) and a subspherical proboscis with 14–16 longitudinal rows of 7–8 hooks. The mud crabs Helice crassa Dana (Grapsidae) and Macrophthalmus hirtipes (Heller) (Ocypodidae) were also harbouring cystacanths and the bar-tailed godwit Limosa lapponica (Linnaeus) (Scolopacidae) juveniles of P. novaezelandensis. This is the first record of brachyuran decapods as intermediate hosts of Acanthocephala from New Zealand. P. antarcticus is recorded from three crab species (Helice crassa, Hemigraspus crenulatus and Macrophthalmus hirtipes) and two bird species (Haematopus o. finschi and Limosa lapponica) in New Zealand. An unidentified species of Plagiorhynchus was also found in two bird species (H. o. finschi and H. unicolor Forster). P. antarcticus and P. novaezelandensis are the first records of Profilicollis from New Zealand.     

Morphological and molecular evidence on the existence of a single estuarine and rocky intertidal acanthocephalan species of <Emphasis Type="Italic">Profilicollis</Emphasis> Meyer, 1931 (Acanthocephala: Polymorphidae) along the Atlantic and Pacific coasts of southern South America

Profilicollis chasmagnathi Holcman-Spector, Mañé-Garzón & Dei-Cas, 1977 (Acanthocephala: Polymorphidae) has been reported to parasitise different grapsid species as intermediate hosts along the South Atlantic shores, i.e. Cyrtograpsus angulatus (Dana) and Neohelice granulata (Dana) in Uruguay and Cyrtograpsus altimanus (Rathbun) in Argentina. Larvae of a similar acanthocephalan described as Profilicollis antarcticus Zdzitowiecki, 1985 were recorded in the crab Hemigrapsus crenulatus (Milne-Edwards) from an estuarine habitat on the Southeast Pacific shore in Chile. Earlier studies have questioned the specific assignation of the Chilean estuarine populations of Profilicollis Meyer, 1931. The aim of this study was to re-examine the identification of these acanthocephalans by means of morphological and molecular analyses of cystacanths of Profilicollis spp. gathered from C. angulatus, N. granulata, C. altimanus and H. crenulatus. Our analyses showed that a single species of Profilicollis, P. chasmagnathi, parasitises these four crab species. The assessment of specimens from the South Shetlands Islands, the type-locality of P. antarcticus, is needed before formally proposing that P. antarcticus is a junior subjective synonym of P. chasmagnathi.     

Phylogenetic relationships, character evolution, and taxonomic implications within the slipper lobsters (Crustacea: Decapoda: Scyllaridae)

The slipper lobsters belong to the family Scyllaridae which contains a total of 20 genera and 89 species distributed across four subfamilies (Arctidinae, Ibacinae, Scyllarinae, and Theninae). We have collected nucleotide sequence data from regions of five different genes (16S, 18S, COI, 28S, H3) to estimate phylogenetic relationships among 54 species from the Scyllaridae with a focus on the species rich subfamily Scyllarinae. We have included in our analyses at least one representative from all 20 genera in the Scyllaridae and 35 of the 52 species within the Scyllarinae. Our resulting phylogenetic estimate shows the subfamilies are monophyletic, except for Ibacinae, which has paraphyletic relationships among genera. Many of the genera within the Scyllarinae form non-monophyletic groups, while the genera from all other subfamilies form well supported clades. We discuss the implications of this history on the evolution of morphological characters and ecological transitions (nearshore vs. offshore) within the slipper lobsters. Finally, we identify, through ancestral state character reconstructions, key morphological features diagnostic of the major clades of diversity within the Scyllaridae and relate this character evolution to current taxonomy and classification.     

La famille des Cicerinidae (Turbellaria, Kalyptorhynchia)

The present study deals with 12 species of Cicerinidae. Further details are given for 6 species previously described: Toia ycia Marcus, Cicerina eucentrota Ax, Nan-norhynchides vividus Brunet, JV. harparius Brunet, N. corneus Brunet, Didiadema picardi Brunet. Two new species are described, Toia calceformis sp.n., different from T. ycia by half-boot shape of the cirrus, and Paracicerina globulosa sp.n., characterized by very short (4 μm) cuticular spermatic ducts and a spherical copulatory bulb provided with a spiny cirrus (35–40 μm long). Histological studies of Ptyalorhynchus coecus Ax confirm the generic separation of Ptyalorhynchus and Paracicerina; the main difference is the glandular girdle structure of the proboscis in Ptyalorhynchus which is split into two areas (inner and outer one) by basal circular muscles; the intensively stained secretion of the inner area is localized in 15 membranous canals. Pocillorhynchus gen.n., with two species, P. agilis sp.n. and P. minutus sp.n., is closely related to the genera Toia and Nannorhynchides , but differs from them by the following characters: proboscis with broad glandular girdle, devoid of circular muscle bulb, cuticular spermatic ducts long and thin (95–125 μm). From the comparison of their morphological and anatomical features, two groups of genera are distinguished in Cicerinidae; first group including Toia - Nannorhynchides - Pocillorhynchus , second group including Cicerina - Paracicerina - Etmorhynchus - Ptyalorhynchus - Zonorhynchus - Xenocicerina - Didiadema. Special attention is paid to proboscis structure. The study ends with an identification key for all known Cicerinidae.     

Behavioral Adaptations to Pollen-Feeding in Heliconius Butterflies (Nymphalidae, Heliconiinae): An Experiment Using Lantana Flowers

Butterflies in the genera Heliconius and Laparus obtain fitness-related benefits from using amino acids derived from pollen. These butterflies have morphological features of the proboscis that facilitate pollen-feeding. Here we investigate behavioral characteristics potentially involved in pollen-gathering. Analysis of four behavioral characters showed that pollen-feeding species manipulate Lantana flowers faster and more thoroughly compared to non-pollen-feeding relatives. Although this suggests that pollen-feeding species are potentially more efficient in harvesting pollen, every butterfly tested successfully removed pollen from Lantana and non-pollen-feeding butterflies generally extracted larger amounts of pollen than Heliconius and Laparus. Morphological characteristics of the proboscis and the production of abundant fluid exudate help keep pollen attached in the proboscis for long periods of time—possibly key to Heliconius' and Laparus' ability to obtain amino acids from pollen. Our results, in concert with those of previous morphological analysis, indicate that behavioral and structural attributes associated with pollen-feeding in Heliconius and Laparus are subtle modifications of widespread butterfly characteristics and raise the question why other butterflies do not use pollen in their diet.     

A molecular assessment of phylogenetic relationships and lineage accumulation rates within the family Salamandridae (Amphibia, Caudata)

We examine phylogenetic relationships among salamanders of the family Salamandridae using approximately 2700 bases of new mtDNA sequence data (the tRNALeu, ND1, tRNAIle, tRNAGln, tRNAMet, ND2, tRNATrp, tRNAAla, tRNAAsn, tRNACys, tRNATyr, and COI genes and the origin for light-strand replication) collected from 96 individuals representing 61 of the 66 recognized salamandrid species and outgroups. Phylogenetic analyses using maximum parsimony and Bayesian analysis are performed on the new data alone and combined with previously reported sequences from other parts of the mitochondrial genome. The basal phylogenetic split is a polytomy of lineages ancestral to (1) the Italian newt Salamandrina terdigitata, (2) a strongly supported clade comprising the "true" salamanders (genera Chioglossa, Mertensiella, Lyciasalamandra, and Salamandra), and (3) a strongly supported clade comprising all newts except S. terdigitata. Strongly supported clades within the true salamanders include monophyly of each genus and grouping Chioglossa and Mertensiella as the sister taxon to a clade comprising Lyciasalamandra and Salamandra. Among newts, genera Echinotriton, Pleurodeles, and Tylototriton form a strongly supported clade whose sister taxon comprises the genera Calotriton, Cynops, Euproctus, Neurergus, Notophthalmus, Pachytriton, Paramesotriton, Taricha, and Triturus. Our results strongly support monophyly of all polytypic newt genera except Paramesotriton and Triturus, which appear paraphyletic, and Calotriton, for which only one of the two species is sampled. Other well-supported clades within newts include (1) Asian genera Cynops, Pachytriton, and Paramesotriton, (2) North American genera Notophthalmus and Taricha, (3) the Triturus vulgaris species group, and (4) the Triturus cristatus species group; some additional groupings appear strong in Bayesian but not parsimony analyses. Rates of lineage accumulation through time are evaluated using this nearly comprehensive sampling of salamandrid species-level lineages. Rate of lineage accumulation appears constant throughout salamandrid evolutionary history with no obvious fluctuations associated with origins of morphological or ecological novelties.     

Systematics of Gagea and Lloydia (Liliaceae) and infrageneric classification of Gagea based on molecular and morphological data

Our study represents the first phylogenetic analyses of the genus Gagea Salisb. (Liliaceae), including 58 species of Gagea and 6 species of the closely related genus Lloydia Salisb. ex Rchb. Our molecular results support the infrageneric classification of the genus Gagea in sections according to Levichev and demonstrate that Pascher's subdivision of this genus into two subgenera can no longer be upheld. Certain Gagea sections (e.g., Gagea, Minimae, and Plecostigma) are well supported by cpDNA and nrDNA data. Gagea sect. Fistulosae is closely related to G. sect. Didymobolbos. Gagea sect. Graminifoliae and G. sect. Incrustatae are closely related to G. sect Platyspermum. The analyses support the monophyly of Gagea and Lloydia collectively. The molecular analyses reveal the basal position of G. graeca in proportion to all other species of Gagea and Lloydia investigated. Minor morphological differences could be established between both genera which support their close relationship.     

Phylogeny of the Baldratiina (Diptera: Cecidomyiidae) inferred from morphological, ecological and molecular data sources, and evolutionary patterns in plant-galler relationships

The phylogeny of the gall-midge subtribe Baldratiina (Diptera: Cecidomyiidae) was reconstructed from molecular (partial sequence of the mitochondrial 12S rDNA), morphological and ecological data sets, using 16 representative species of most of the genera. The morphological and ecological data were combined in a single character matrix and analyzed separately from the molecular data, resulting in an eco-morphological cladogram and a molecular cladogram. Attributes of galls and host associations were superimposed on the molecular cladogram in order to detect possible trends in the evolution of these traits. The cladograms resulting from the two independent analyses were statistically incongruent, although both provide evidence for the monophyly of the genera Baldratia and Careopalpis and the paraphyly of the genera Stefaniola and Izeniola. The results suggest a minor impact of the morphological characters traditionally used in the classification of the Baldratiina, whereas ecological data had a major impact on the phylogenetic inference. Mapping of gall and host attributes on the molecular cladogram suggests that multi-chambered stem galls constitute the ancestral state in the subtribe, with several subsequent shifts to leaf galls. It is concluded that in contrast to other studied groups of gall insects, related baldratiine species induce different types of galls, attesting to speciation driven by gall-type shifts at least as often as host shifts.     

TRADITIONAL GENERIC CONCEPTS VERSUS 18S rRNA GENE PHYLOGENY IN THE GREEN ALGAL FAMILY SELENASTRACEAE (CHLOROPHYCEAE, CHLOROPHYTA)

Coccoid green algae of the Selenastraceae were investigated by means of light microscopy, TEM, and 18S rRNA analyses to evaluate the generic concept in this family. Phylogenetic trees inferred from the 18S rRNA gene sequences showed that the studied species of autosporic Selenastraceae formed a well-resolved monophyletic clade within the DO group of Chlorophyceae. Several morphological characteristics that are traditionally used as generic features were investigated, especially the arrangement of autospores in the mother cells, colony formation, and pyrenoid structure. The parallel arrangement of autospores was confirmed for the genera Ankistrodesmus , Podohedriella , and Quadrigula. In mother cells of Monoraphidium and Kirchneriella , the autospores were arranged serially. Colony formation was either stable ( Quadrigula ) or variable ( Ankistrodesmus , Podohedriella ) within genera. All strains studied possessed naked or starch-covered pyrenoids within the chloroplast. The pyrenoid matrix was homogenous or penetrated by thylakoids. In contrast to considerations of traditional systematics, the present study showed that the presence and structure of pyrenoids are unsuitable for differentiation of genera in Selenastraceae. Furthermore, the molecular analyses showed that any morphological criterion considered so far is not significant for the systematics of the Selenastraceae on the generic level. Species assigned to different genera such as Ankistrodesmus and Monoraphidium were not monophyletic and therefore not distinguishable as separate genera. Species of Monoraphidium appeared in four different lineages of the Selenastraceae. Our phylogenetic analyses support earlier discussions to abandon the common practice of conceiving "small" genera (i.e. genera that are differentiated from other genera by only a few diacritic characteristics and that contain only a small number of species) and to reestablish "large" genera of Selenastraceae such as Ankistrodesmus.     

Re-assessment of monophyly, evolution of myrmecophytism, and rapid radiation in Neonauclea s.s. (Rubiaceae)

The biologically interesting ant-plant association, myrmecophytism, occurs in ca. 140 of the 11,000 species and 22 of the 630 genera of the coffee family (Rubiaceae). These myrmecophytic Rubiaceae species are predominantly distributed in Southeast Asia, especially the Malesian region, with comparatively few species in mainland Africa and the Neotropics. The mostly Southeast Asian genus Neonauclea s.s is one of the three Rubiaceae genera with extensive radiation of myrmecophytes and also the most speciose genus of the tribe Naucleeae s.l. We perform parsimony phylogenetic analyses of Neonauclea s.s., previously resolved as paraphyletic, and its allied genera using both ETS and ITS sequencing data to test: (1) the paraphyly of Neonauclea s.s.; (2) the phylogenetic relationships within the Ludekia-Myrmeconauclea-Neonauclea complex; and (3) the evolution of myrmecophytism within the complex. The earlier proposed paraphyly of Neonauclea s.s. appears to be the result of the combined effects of parallel substitutions in Metadina trichotoma and the sampled ITS putative pseudogenes of Neonauclea longipedunculata and losses of some synapomorphies of Neonauclea s.s. in the latter. The analyses present strong support for the monophyly of Myrmeconauclea and Neonauclea s.s. and their sister-group relationships. Our findings additionally favor the hypothesis of multiple origins of myrmecophytism in the Bornean Neonauclea, which have independently been exploited by at least three Cladomyrma ant species. Furthermore, we interpret the low levels of variation in both the ETS and ITS sequences as indication of a recent and rapid radiation for Neonauclea s.s. (with 65 species) and a recent and slow radiation for Myrmeconauclea (with three species). We argue that the rapid diversification of Neonauclea s.s. is partly associated with the nature of its fruits and its ability to colonize a wide range of habitats. We postulate that both ecological and geographical events may have been responsible for the radiation of the non-myrmecophytic Neonauclea species. Finally, we argue that the acquisition of the pseudo-multiple fruits and long-tailed seeds has allowed Myrmeconauclea to specialize on rheophytic habitats but its narrow ecological tolerance may have hindered its speciation.