Evolutionary trends in body size of parasitic flatworms

Evolutionary trends in body size have been identified within several lineages, but not all have followed Cope's rule, which states that average body size within a taxon tends to increase over time. In organisms such as parasites, space constraints may have shaped the evolution of body sizes, favouring small-bodied taxa capable of exploiting new niches. Here, the average adult body sizes of families in three groups of parasitic flatworms, the Digenea and two clades of Monogenea (Monopisthocotylea and Polyopisthocotylea), are related to their clade rank. Clade rank reflects the number of branching events, and thus the total path length, between an extant family and the root of the phylogenetic tree. Among families of Digenea, all of which are endoparasites of vertebrates, there was no trend in body size evolution. In contrast, the Monopisthocotylea and Polyopisthocotylea, which are (with the exception of Polystomatidae and Sphyranuridae) ectoparasites of fish, revealed significant negative relationships between family body size and clade rank, suggesting an evolutionary trend of decreasing size. In addition, an analysis of body size distributions in monogenean families also provides support, albeit weak, for this trend. From an ancestor parasitic on the skin of fishes, monogeneans have diversified by colonizing other microhabitats on their hosts, including such space-limited sites as the gaps between secondary gill lamellae. Using a conservative likelihood ratio test, however, a random walk, or null model of evolution could not be discarded in favour of the directional trends mentioned above. Nevertheless, these results suggest that body size has taken different evolutionary paths in endo- and ectoparasitic flatworms.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 181–189.     

Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea)

The evolution and determinants of host specificity in Lamellodiscus species (Monogenea, Diplectanidae) were investigated. The 20 known Mediterranean species were studied, all parasites of fishes from the family Sparidae (Teleostei). An index of specificity, which takes into account the phylogenetic relationships of their fish host species, was defined. The link between specificity and its potential determinants was investigated in a phylogenetic context using the method of independent contrasts. Host specificity in Lamellodiscus species appeared to be highly constrained by phylogeny, but also linked to host size. Mapping specificity onto the parasite phylogenetic tree suggests that specialist species do not represent an evolutionary dead end, and that specialization is not a derived condition. It is hypothesized that the ability to be generalist or specialist in Lamellodiscus is controlled by intrinsic, phylogenetically-related characteristics, and that specialist species tend to use large hosts, which may be more predictable.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77, 431−443.     

The eyespots of the oncomiracidium of Euzetrema knoepffleri (Monogenea): ultrastructure and evolution during the life-cycle (author's transl)]

Euzetrema knoepffleri (Monogenea, Monopisthocotylea) is a parasite of the urinary bladder of Euproctus montanus (Amphibia, Urodela). The eyespots of the oncomiracidium of E. knoepffleri are rhabdomeric; each anterior pigmented cell has one rhabdomere, each posterior pigmented cell has two rhabdomeres. This pattern is quite similar to that of the eyespot of another Monopisthocotylea, Entobdella soleae but the lack of cristalline lens in E. knoepffleri appears as a new feature of the Monopisthocotylea. The symmetry of the pigmented structures seems to be effectively connected with the swimming mode of the larva. Moreover, the ultrastructural differences between the two species Euzetrema knoepffleri and Entobdella soleae may be in relation with their different behaviour concerning light. After the fixation of the larva on its host, the comparative study of the evolution of the eyespots, shows the disappearance of the cristalline lens in Entobdella, and the loss of rhabdomeric structures in Euzetrema. These differences seem related with the nature of the microbiotope of the adult: Entobdella soleae is a skin parasite, Euzetrema knoepffleri a reno-vesical one.     

Phylogeny of the monopisthocotylea and Polyopisthocotylea (Platyhelminthes) inferred from 28S rDNA sequences

This study focuses on the phylogenetic relationships within the Polyopisthocotylea and Monopisthocotylea, two groups that are often grouped within the monogeneans, a group of disputed paraphyly. Phylogenetic analyses were conducted with multiple outgroups chosen according to two hypotheses, a paraphyletic Monogenea or a monophyletic Monogenea, and with three methods, namely maximum parsimony, neighbour joining and maximum likelihood. Sequences used were from the partial domain C1, full domain D1, and partial domain C2 (550 nucleotides, 209 unambiguously aligned sites) from the 28S ribosomal RNA gene for 16 species of monopisthocotyleans, 26 polyopisthocotyleans including six polystomatids, and other Platyhelminthes (61 species in total, 27 new sequences). Results were similar with outgroups corresponding to the two hypotheses. Within the Monopisthocotylea, relationships were: ?[(Udonella, capsalids), monocotylids], (diplectanids, ancyrocephalids)?; each of these families was found to be monophyletic and their monophyly was supported by high bootstrap values in neighbour joining and maximum parsimony. Within the Polyopisthocotylea, the polystomatids were the sister-group of all others. Among the latter, Hexabothrium, parasite of chondrichthyans, was the most basal, and the mazocraeids, mainly parasites of clupeomorph teleosts, were the sister-groups of all other studied polyopisthocotyleans, these, mainly parasites of euteleosts, being polytomous.     

False Vertical Rootlets of Epidermal Cilia in the Oncomiracidia of Neoheterocotyle rhinobatidis and Monocotyle spiremae (Platyhelminthes,Monogenea, Monopisthocotylea)

Epidermal cilia of the oncomiracidium of Neoheterocotyle rhinobatidis (Monogenea, Monopisthocotylea, Monocotylidae) have long cross-striated vertical rootlets that are not extensions of the basal bodies as are the vertical rootlets in all catenulid and rhabditophoran turbellarians examined to date. Instead, they originate in the basal part of the horizontal rootlet a short distance from the basal bodies. In Monocotyle spiremae (Monocotylidae), the vertical rootlets are less distinct, with no apparent cross-striation, but they also originate from the basal part of the horizontal rootlets. Epidermal cilia of the oncomiracidium of Zeuxapta seriolae (Monogenea, Polyopisthocotylea, Axinidae) lack vertical rootlets like all other neodermatans examined, but bundles of fibres extend from the basal bodies a short distance into the cytoplasm of the epidermal cells. Monopisthocotylean Monogenea would be intermediate between rhabditophorans and the other neodermatans (in having weakly developed vertical rootles), if these structures were homologous in the two groups. However, in view of the different origin of vertical rootlets in turbellarians and monopisthocolylean oncomiracidia, it is suggested that they are not homologous, and vertical rootlets in the Monopisthocotylea are therefore named “false vertical rootlets”.     

Ecological approach to the problem of monophyly of Neodermata (Platyhelminthes)

The ecological scenario of the evolution of main branches of Neodermata is described. The first neodermateans (= promonogeneans) were parasites of the gill lamellae of Paleozoic jawless vertebrates, which were microphagous suspension-feeding animals. The main apomorphic characters of the primary neodermateans are neodermis, cercomer (posterior hooked attachment organ) and swimming infective larva. All subsequent evolution of Neodermata was related with their acquisition new niches in hosts, which were intensively diverging in that time adapting to new food types and conquering new ecological niches. The acquisition of new microhabitats was accompanied by the development of morphological diversity in Neodermata especially in a structure of attachment and genital organs. Trematoda, Cestoda and Polyopisthocotylea comprise specialized evolutionary lineages and Monopisthocotylea is a basal taxon. Polyopisthocotylea is specialized to the blood feeding on fish gills. The common ancestors of the Trematoda and Cestoda inhabited walls of gills and pharyngeal cavities, from where they penetrated the digestive tract. The aspidogastridean multiloculate hold fast appears to be a highly specialized attachment organ of the monogenean ancestor, which inhabited muscular pharyngeal walls of Paleozoic vertebrates. The loss of cercomer hooks probably took place when mollusk-hosts have been involved in the aspidogastridean life cycle. The extinction of many chondrichthiean groups and progress of small plankton fishes (Teleostei) has led to the appearance Digenea. New vertebrate hosts needed a new infestation type and the cercaria appeared. Parthenogenesis has been developed in stages living in mollusks to counterbalance the loss of individuals at two transmission stages in the digenean cycle; this was resulted in a strong specificity to mollusk-host. Evolutionary tendencies of Trematoda and Cestoda show noticeable similarities.     

Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo

Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 551–563.     

Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory

We combined nearly complete sequences of large (LSU) and small (SSU) subunit rDNA from 32 flatworm species to estimate the phylogeny of the Platyhelminthes using maximum parsimony, maximum likelihood and Bayesian inference methods. Rooted against the Catenulida, combined evidence trees offered no support for the Revertospermata, which was also rejected by constraint analysis. Generally, nodal support was higher for groupings estimated from the combined data partitions and all methods of analysis provided congruent estimates of phylogeny. The Monogenea and Proseriata were resolved as monophyletic, rejecting previous suggestions of paraphyly based on SSU and partial LSU data sets and thus supporting widely accepted morphological synapomorphies. Monophyly of the Neodermata was supported and its sister group was a clade of neoophoran 'turbellarians' to the exclusion of the Proseriata which in turn was more basal. Taxa with similar spermatology to the Neodermata ( Ichthyophaga , Notentera , Urastoma and Kronborgia ) were the sister group to Tricladida + Prolecithophora, which in turn were sister to the Rhabdocoela. Polycladida + Macrostomida + Lecithoepitheliata was the earliest divergent offshoot of the Rhabditophora. Among the Neodermata, the Cercomeromorphae (Cestoda + Monogenea) was not supported, whereas Cestoda + Trematoda was well supported. Although there is no known synapomorphy for this latter grouping, our data highlight problems associated with the 'cercomer theory' and we reject putative homologies regarding neodermatan 'cercomers' that have been sustained in the literature without careful scrutiny.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78, 155–171.     

Encounter rate between local populations shapes host selection in complex parasite life cycle

The present study aimed to understand how a parasite with a complex life cycle selects a given host succession when several potential hosts are present. Ligula intestinalis (Cestoda, Pseudophyllidea) was considered, which presents a life cycle with three hosts: copepod, fish, and piscivorous bird. Encounter probability between each pair of hosts was calculated for Lavernose-Lacasse gravel pit (France) using a sum of the product of the host abundances over time. Among four potential copepod hosts, two potential fish hosts, and six potential bird hosts, the results demonstrate that the copepod Eudiaptomus gracilis , the roach ( Rutilus rutilus ), and the great crested grebe ( Podiceps cristatus ) had a maximal encounter probability due to their abundance, but also due to the similarities of the temporal dynamics of their life cycles. These results agree with previous experiments and field work identifying a high specificity of L. intestinalis to E. gracilis , R. rutilus , and P. cristatus in the study site. This suggests that the abundance of potential hosts and the temporal dynamics of their life cycles act together to determine encounter rates between hosts and parasites, and thus could constitute a crucial determinant in local host selection by parasites with a complex life cycle.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 99–106.     

First discovery of a primitive coelacanth fin fills a major gap in the evolution of lobed fins and limbs

The fossil record provides unique clues about the primitive pattern of lobed fins, the precursors of digit-bearing limbs. Such information is vital for understanding the evolutionary transition from fish fins to tetrapod limbs, and it guides the choice of model systems for investigating the developmental changes underpinning this event. However, the evolutionary preconditions for tetrapod limbs remain unclear. This uncertainty arises from an outstanding gap in our knowledge of early lobed fins: there are no fossil data that record primitive pectoral fin conditions in coelacanths, one of the three major groups of sarcopterygian (lobe-finned) fishes. A new fossil from the Middle-Late Devonian of Wyoming preserves the first and only example of a primitive coelacanth pectoral fin endoskeleton. The strongly asymmetrical skeleton of this fin corroborates the hypothesis that this is the primitive sarcopterygian pattern, and that this pattern persisted in the closest fish-like relatives of land vertebrates. The new material reveals the specializations of paired fins in the modern coelacanth, as well as in living lungfishes. Consequently, the context in which these might be used to investigate evolutionary and developmental relationships between vertebrate fins and limbs is changed. Our data suggest that primitive actinopterygians, rather than living sarcopterygian fishes and their derived appendages, are the most informative comparators for developmental studies seeking to understand the origin of tetrapod limbs.     

Modularity in attachment organs of African Cichlidogyrus (Platyhelminthes: Monogenea: Ancyrocephalidae) reflects phylogeny rather than host specificity or geographic distribution

Cichlidogyrus spp. (Monogenea, Ancyrocephalidae) are common parasites of cichlid fishes from Africa and the Levant. They display important morphological variation in their attachment apparatus and infect a broad host spectrum throughout a wide geographic range. Thus, they offer an interesting model to investigate to what extent the phenotypic variability of the attachment organ among congeners is related to host specificity, geographic/environmental components, or phylogeny. A geometric morphometric approach was carried out to analyse the shape variation of sclerotized structures of the attachment organ within 66 African species of the genus Cichlidogyrus. The interspecific shape comparison supports the presence of three main morphological configurations, each consisting of a given combination of particular sclerite shapes. Moreover, data emphasize strong coordination and integration (shape co‐variation) among the different sclerites jointly forming the attachment organ. Although attachment apparatuses are usually considered to be the result of adaptive processes and must be adapted to the hosts and local environmental conditions, we found no relationship between these clusters and host specificity or geographical distribution. Nevertheless, groups are partially congruent with those obtained with the molecular phylogeny of a subset of species, suggesting a phylogenetic constraint rather than an adaptation to either hosts or environment. Because of the necessity to form a functional entity, modularity within attachment organ imposes important evolutionary constraint. This provides new insights into the evolvability of attachment organs, as well as into the morphological basis of host specificity and host–parasite co‐evolutionary interaction in helminth parasites. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 694–706.     

Spread of parasites and diseases of aquatic organisms by acclimatization: a short review

The influence of transportation and acclimatization of fishes and shellfishes on their parasites and pathogens is discussed. It has been shown that aquatic organisms lose most of their parasites during the period of establishment, but some species may remain. In most instances these are parasites with direct development (Myxosporea, Monogenea, Crustacea). Species with intermediate hosts, but which utilize many species of invertebrates, establish more easily than those which have specific invertebrate intermediate hosts. If there are closely related host species to those introduced into the water body, parasites brought to it can transfer to these related species. This may result in a high infection of the native species and significant mortality.     

The diversity of hemi-epiphytic figs (Ficus ; Moraceae) in a Bornean lowland rain forest

The diversity and niche specificity of hemi-epiphytic figs in a lowland dipterocarp forest in Sarawak were investigated in 1998. Twenty-seven fig species (264 individuals, c. 120 ha) colonized a diversity of host taxa (35 families), but densities were very low and only 1.77% of trees> 30 cm d.b.h. were occupied. There were no significant associations with host taxa or host-bark roughness but among 11 common species (≥9 individuals) the distributions of all other parameters (host-d.b.h., height and position of colonization, crown illumination, soil-texture and slope-angle) were significantly different, and we identified five fig guilds. The guilds corresponded to canopy strata, and appeared to reflect the establishment microsite requirements of different species. A fundamental trade-off within the hemi-epiphytic habit was revealed: Species colonizing larger hosts were rarer, because of lower host densities and more specific microsite requirements, but had better light environments and attained a larger maximum size. The single strangler species appeared to escape many of these constraints, and an important source of mortality caused by host-toppling, indicating the advantages of this strategy. Thus, the hemi-epiphytic figs in this community have come to fill a remarkable diversity of niches, despite low levels of competition, through the exigencies of a complex environment.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 78 , 439–455     

Mimicry vs. similarity: which resemblances between brood parasites and their hosts are mimetic and which are not?

Mimicry is one of the most conspicuous and puzzling phenomena in nature. The best-known examples come from insects and brood parasitic birds. Unfortunately, the term 'mimicry' is used indiscriminately and inconsistently in the brood parasitic literature despite the obvious fact that similarities of eggs, nestlings and adults of brood parasites to their hosts could result from many different processes (phylogenetic constraint, predation, intraspecific arms-races, vocal imitation, exploitation of pre-existing preferences, etc.). In this note I wish to plead for a more careful use of the term. I review various processes leading to a similarity between propagules (both eggs and nestlings) of brood parasites and their hosts and stress that: (1) mimetic and non-mimetic similarities should be differentiated, (2) a mere similarity of host and parasite propagules provides no evidence for mimicry, (3) mimicry is more usefully understood as a (coevolutionary) process rather than an appearance, and (4) mimicry terminology should reflect the process which led to mimetic similarity. Accepting the mimicry hypothesis requires both the experimental approach and rejection of alternative hypotheses explaining similarities of host and parasite propagules.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 69–78.     

A new species of Hybanthus (Violaceae) from north-eastern Brazil

A new species of Hybanthus (Violaceae) from north-eastern Brazil is described and illustrated. Hybanthus verrucosus Paula-Souza is endemic to 'caatingas' of Bahia and Alagoas states and is very distinct from all other Brazilian species of the genus, for its anterior petal, which is covered with small wart-like outgrowths. Other distinctive characteristics of the new species and its relationship with a closely related species ( H. atropurpureus (A.St.-Hil.) Taub.) are discussed.  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 141 , 503–506.     

Southern African pholcid spiders: revision and cladistic analysis of Quamtana gen. nov. and Spermophora Hentz (Araneae: Pholcidae), with notes on male−female covariation

The southern African pholcid spiders previously assigned to Pholcus and Spermophora are revised and their phylogenetic position within Pholcidae is analysed cladistically. Two distinct groups are recognized: the first is restricted to the Cape region and probably correctly placed in Spermophora ; it includes Spermophora peninsulae Lawrence and four new species. The second is more widely distributed in southern and eastern South Africa, and reaches as far north as Cameroon, Congo (Democratic Republic) and Uganda; it is assigned generic status ( Quamtana gen. nov .), and includes two species transferred from Pholcus [ Q. leptopholcica (Strand), Q. ciliata (Lawrence)] as well as 23 new species. A key to the pholcid spiders of South Africa is presented. A close correlation between a male character (distance between cheliceral apophyses) and a female character (distance between pockets on epigynum) is documented in Quamtana .  © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society, 2003, 139 , 477−527.     

A phylogeny of the families of fossil and extant tetraodontiform fishes (Acanthomorpha, Tetraodontiformes), Upper Cretaceous to Recent

A data matrix is presented of 210 morphological characters (mostly osteological, some external) for 20 extant taxa of the ten Recent families of tetraodontiform fishes and 36 fossil tetraodontiforms. The oldest of these are from the Upper Cretaceous (95 Mya); most are from the Lower to Middle Eocene (50–58 Mya). There are two outgroup taxa (a zeiform and a caproid). A cladistic analysis of this matrix for only the extant taxa produced two equally parsimonious trees that call into question the monophyly of some of the previously accepted major higher-level tetraodontiform clades. Inclusion in the analysis of the large number of available fossil taxa helps to resolve relationships between family level clades. The new phylogenetic hypothesis, together with stratigraphic and biogeographical data, is used to discuss scenarios of the origin and evolution of the major clades of the order.  © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society , 2003, 139 , 565−617.     

Richness and endemism of helminth parasites of freshwater fishes in Mexico

Distribution records of 152 adult helminth taxa parasites of freshwater fishes in Mexico were analysed to determine areas of high richness and endemism. Distribution maps were prepared for each taxon and overlaid onto a map of Mexico divided into 1 × 1 degree grid-cells. Richness was determined by counting recorded helminth species in each grid-cell. A corrected weighted endemism index was calculated for each grid-cell, and the relationship between richness and endemicity was analysed with an Olmstead–Tukey corner test of association. Five areas of high richness and endemism were identified: (1) Los Tuxtlas and the Papaloapan river basin, on the Gulf of Mexico; (2) the Grijalva-Usumacinta basin near the Gulf of Mexico coastal plain; (3) the Yucatan Peninsula; (4) the Sierra de Manantlán Biosphere Reserve in western Mexico; and (5) the Pátzcuaro lake, in central Mexico. The distribution of richness and endemism of helminth parasites of freshwater fishes in Mexico is congruent with distributional patterns described for other freshwater taxa in Mexico. Patterns of richness and/or endemism in the studied areas can be explained by the ichthyological composition of their bodies of water. The present study establishes an objective way of analysing the relationship between richness and endemicity, and suggests that helminths can make valuable contributions to regionalization of geographical areas and for identification of rich and biologically complex areas with potential for conservation of aquatic systems.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 435–444.