Migration strategy and pathogen risk: non‐breeding distribution drives malaria prevalence in migratory waders

Pathogen exposure has been suggested as one of the factors shaping the myriad of migration strategies observed in nature. Two hypotheses relate migration strategies to pathogen infection: the ‘avoiding the tropics hypothesis’ predicts that pathogen prevalence and transmission increase with decreasing non‐breeding (wintering) latitude, while the “habitat selection hypothesis” predicts lower pathogen prevalence in marine than in freshwater habitats. We tested these scarcely investigated hypotheses by screening wintering and resident wading shorebirds (Charadriiformes) for avian malaria blood parasites (Plasmodium and Haemoproteus spp.) along a latitudinal gradient in Australia. We sequenced infections to determine if wintering migrants share malaria parasites with local shorebird residents, and we combined prevalence results with published data in a global comparative analysis. Avian malaria prevalence in Australian waders was 3.56% and some parasite lineages were shared between wintering migrants and residents, suggesting active transmission at wintering sites. In the global dataset, avian malaria prevalence was highest during winter and increased with decreasing wintering latitude, after controlling for phylogeny. The latitudinal gradient was stronger for waders that use marine and freshwater habitats (marine + freshwater) than for marine‐restricted species. Marine + freshwater wader species also showed higher overall avian malaria parasite prevalence than marine‐restricted species. By combining datasets in a global comparative analysis, we provide empirical evidence that migratory waders avoiding the tropics during the non‐breeding season experience a decreased risk of malaria parasite infection. We also find global support for the hypothesis that marine‐restricted shorebirds experience lower parasite pressures than shorebirds that also use freshwater habitats. Our study indicates that pathogen transmission may be an important driver of site selection for non‐breeding migrants, a finding that contributes new knowledge to our understanding of how migration strategies evolve.     

A recent marine ancestry for diadromous fishes? Sometimes yes,but mostly no!

Synopsis Diadromy in its three forms (anadromy, catadromy and amphidromy) necessarily involves fish spending part of their lives in the sea. It is not uncommon contention that diadromous fish have a recent marine ancestry and that they are in the process of moving from a marine to a freshwater lifestyle. However, analysis of the distribution of diadromy in fishes suggests that, for most species, it is an ancient life history style though, for a few, a recent marine ancestry seems plausible. In general, there is no reason to consider diadromy anything but a stable and successful life history style, and no reason to regard it as transitional between marine and freshwater habitats.Invited Editorial     

DO FRESHWATER FISHES DIVERSIFY FASTER THAN MARINE FISHES? A TEST USING STATE‐DEPENDENT DIVERSIFICATION ANALYSES AND MOLECULAR PHYLOGENETICS OF NEW WORLD SILVERSIDES (ATHERINOPSIDAE)

Freshwater habitats make up only ～0.01% of available aquatic habitat and yet harbor 40% of all fish species, whereas marine habitats comprise >99% of available aquatic habitat and have only 60% of fish species. One possible explanation for this pattern is that diversification rates are higher in freshwater habitats than in marine habitats. We investigated diversification in marine and freshwater lineages in the New World silverside fish clade Menidiinae (Teleostei, Atherinopsidae). Using a time‐calibrated phylogeny and a state‐dependent speciation–extinction framework, we determined the frequency and timing of habitat transitions in Menidiinae and tested for differences in diversification parameters between marine and freshwater lineages. We found that Menidiinae is an ancestrally marine lineage that independently colonized freshwater habitats four times followed by three reversals to the marine environment. Our state‐dependent diversification analyses showed that freshwater lineages have higher speciation and extinction rates than marine lineages. Net diversification rates were higher (but not significant) in freshwater than marine environments. The marine lineage‐through time (LTT) plot shows constant accumulation, suggesting that ecological limits to clade growth have not slowed diversification in marine lineages. Freshwater lineages exhibited an upturn near the recent in their LTT plot, which is consistent with our estimates of high background extinction rates. All sequence data are currently being archived on Genbank and phylogenetic trees archived on Treebase.     

Multiple invasions into freshwater by pufferfishes (teleostei: tetraodontidae): a mitogenomic perspective

Pufferfishes of the Family Tetraodontidae are the most speciose group in the Order Tetraodontiformes and mainly inhabit coastal waters along continents. Although no members of other tetraodontiform families have fully discarded their marine lives, approximately 30 tetraodontid species spend their entire lives in freshwaters in disjunct tropical regions of South America, Central Africa, and Southeast Asia. To investigate the interrelationships of tetraodontid pufferfishes and thereby elucidate the evolutionary origins of their freshwater habitats, we performed phylogenetic analysis based on whole mitochondrial genome sequences from 50 tetraodontid species and closely related species (including 31 newly determined sequences). The resulting phylogenies reveal that the family is composed of four major lineages and that freshwater species from the different continents are independently nested in two of the four lineages. A monophyletic origin of the use of freshwater habitats was statistically rejected, and ancestral habitat reconstruction on the resulting tree demonstrates that tetraodontids independently entered freshwater habitats in different continents at least three times. Relaxed molecular-clock Bayesian divergence time estimation suggests that the timing of these invasions differs between continents, occurring at 0-10 million years ago (MA) in South America, 17-38 MA in Central Africa, and 48-78 MA in Southeast Asia. These timings are congruent with geological events that could facilitate adaptation to freshwater habitats in each continent.     

Molecular Comparisons of Freshwater and Marine Isolates of the Same Morphospecies of Heterotrophic Flagellates

Heterotrophic flagellates are key components of all ecosystems. Understanding the patterns of biodiversity of these organisms is thus particularly important. Here we analyzed the intraspecific diversity of 10 morphospecies of heterotrophic flagellates comprising representatives of the Apusozoa (2 morphospecies) and Kinetoplastea (8 morphospecies), all belonging to the most common flagellates with worldwide distribution. Most morphospecies showed a mixing of lineages isolated from diverse habitats, indicating that some lineages of these morphospecies had been able to colonize different habitats several times. Furthermore, our results revealed remarkable levels of genetic divergence within most of the morphospecies studied, underlining the difficulty of correctly determining species by means of morphology alone. Many cryptic or pseudocryptic species seem to occur. Our results revealed clear divergence between marine and freshwater lineages of the morphospecies Ancyromonas sigmoides, showing that freshwater lineages have not been able to colonize marine environments and marine lineages have not been able to colonize freshwater environments for a long time.     

Global analysis reveals that cryptic diversity is linked with habitat but not mode of life

The ubiquity of genetically distinct, cryptic species is limiting any attempt to estimate local or global biodiversity as well as impeding efforts to conserve species or control pests and diseases. Environmental factors or biological traits promoting rapid diversification into morphologically similar species remain unclear. Here, using a meta‐analysis of 1230 studies using DNA sequences to search for cryptic diversity in metazoan taxa, we test two hypotheses regarding the frequency of cryptic taxa based on mode of life and habitat. First, after correcting for study effort and accounting for higher taxonomic affinities and biogeographical region of origins, our results do not support the hypothesis that cryptic taxa are more frequent among parasitic than free‐living taxa. Second, in contrast, the results support the hypothesis that cryptic taxa are more common in certain habitats than others: for a given study effort, more cryptic taxa are found in freshwater than in terrestrial or marine taxa. These findings suggest that the greater heterogeneity and fragmentation of freshwater habitats may promote higher rates of genetic differentiation among its inhabitants, a general pattern with serious implications for freshwater conservation biology.     

Molecular comparisons of freshwater and marine isolates of the same morphospecies of heterotrophic flagellates

Heterotrophic flagellates are key components of all ecosystems. Understanding the patterns of biodiversity of these organisms is thus particularly important. Here we analyzed the intraspecific diversity of 10 morphospecies of heterotrophic flagellates comprising representatives of the Apusozoa (2 morphospecies) and Kinetoplastea (8 morphospecies), all belonging to the most common flagellates with worldwide distribution. Most morphospecies showed a mixing of lineages isolated from diverse habitats, indicating that some lineages of these morphospecies had been able to colonize different habitats several times. Furthermore, our results revealed remarkable levels of genetic divergence within most of the morphospecies studied, underlining the difficulty of correctly determining species by means of morphology alone. Many cryptic or pseudocryptic species seem to occur. Our results revealed clear divergence between marine and freshwater lineages of the morphospecies Ancyromonas sigmoides, showing that freshwater lineages have not been able to colonize marine environments and marine lineages have not been able to colonize freshwater environments for a long time.     

Eocene–Oligocene sea-level fall drove amphipod habitat shift from marine to freshwater in the Far East

The Eocene–Oligocene sea-level fall has been viewed as a primary driver of biological succession. We used Anisogammaridae living in both marine and freshwater habitats to test the hypothesis that Eocene–Oligocene sea-level fall can explain the marine–freshwater habitat shift in the Far East. We obtained three mitochondrial and two nuclear fragments for 138 samples representing 31 species, covering marine and freshwater habitats from latitudes 24 to 50°N. The phylogenetic analyses revealed that freshwater Anisogammaridae is monophyletic. Divergence-time estimation and ancestral range reconstruction indicate that the family originated from a marine habitat in the North Pacific region during the Eocene and separated between marine and freshwater lineages at 38 Ma. The freshwater lineage diversified at 27 Ma, and further diverged into lotic and lentic clades. Our results suggest that the Eocene–Oligocene sea-level fall provided an opportunity for marine-derived Anisogammaridae to shift to new freshwater habitats. The freshwater anisogammarids dispersed from north to south, resulting in the restriction of current marine species restricted to the latitudes 35–50°N and the range of freshwater species in latitudes 24–40°N. Deep divergences within the freshwater lineage were related to the separation of lotic and lentic environments and the opening of the Japan Sea.     

Latitudinal trends in adult body size of Dolly Varden, with special reference to the food availability hypothesis

The food availability hypothesis (FAH) predicts that the relative productivity of ocean and freshwater habitats changes with latitude, and that anadromy will evolve when ocean productivity is greater than that in neighboring freshwater habitats, or vice versa. In data sets for the anadromous salmonid species Salvelinus malma, we show that the relative body size at maturity of anadromous populations is much larger in the northern limits of their ranges than that of fluvial populations, and, conversely, that of fluvial populations is slightly smaller at the southern limits than that of anadromous populations, supporting the FAH for the evolution of migration behavior in salmonids. Received: October 4, 2001 / Accepted: January 7, 2002     

Phylogenetic tree of vascular plants reveals the origins of aquatic angiosperms

Although aquatic plants are discussed as a unified biological group, they are phylogenetically well dispersed across the angiosperms. In this study, we annotated the aquatic taxa on the tree of vascular plants, and extracted the topology of these aquatic lineages to construct the tree of aquatic angiosperms. We also reconstructed the ancestral areas of aquatic families. We found that aquatic angiosperms could be divided into two different categories: the four aquatic orders and the aquatic taxa in terrestrial orders. Aquatic lineages evolved early in the radiation of angiosperms, both in the orders Nymphaeales and Ceratophyllales and among basal monocots (Acorales and Alismatales). These aquatic orders do not have any extant terrestrial relatives. They originated from aquatic habitats during the Early Cretaceous. Asia would have been one of the centers for early diversification of aquatic angiosperms. The aquatic families within terrestrial orders may originate from other areas besides Asia, such as America or Australia. The lineages leading to extant angiosperms diversified early in underexploited freshwater habitats. The four extant aquatic orders were relicts of an early radiation of angiosperm in aquatic environments. Their extinct ancestors might be aquatic early angiosperms.     

Out of the blue: adaptive visual pigment evolution accompanies Amazon invasion

Incursions of marine water into South America during the Miocene prompted colonization of freshwater habitats by ancestrally marine species and present a unique opportunity to study the molecular evolution of adaptations to varying environments. Freshwater and marine environments are distinct in both spectra and average intensities of available light. Here, we investigate the molecular evolution of rhodopsin, the photosensitive pigment in the eye that activates in response to light, in a clade of South American freshwater anchovies derived from a marine ancestral lineage. Using likelihood-based comparative sequence analyses, we found evidence for positive selection in the rhodopsin of freshwater anchovy lineages at sites known to be important for aspects of rhodopsin function such as spectral tuning. No evidence was found for positive selection in marine lineages, nor in three other genes not involved in vision. Our results suggest that an increased rate of rhodopsin evolution was driven by diversification into freshwater habitats, thereby constituting a rare example of molecular evolution mirroring large-scale palaeogeographic events.     

Freshwater habitat use by a moray eel species,Gymnothorax polyuranodon,in Fiji shown by otolith microchemistry

Freshwater eels of the Anguillidae are diadromous because they migrate between ocean and freshwater environments, but other anguilliform fishes are generally considered to be strictly marine species. A few marine eels of the Muraenidae and Ophichthidae have occasionally been found in freshwater or estuaries, indicating that anguillids are not the only anguilliform eels that can use freshwater in some parts of the world. The moray eel Gymnothorax polyuranodon is one species that is known to be present in freshwater in the Indo-Pacific, but its life history is unknown. One way to evaluate what types of habitats are used by fishes is to determine the ratio of strontium (Sr) to calcium (Ca) in their otoliths, because this can show if they have used freshwater or saltwater environments. To evaluate the patterns of freshwater use by this unusual species of marine eel, the otolith Sr/Ca ratios of four G. polyuranodon (275–344 mm) caught in a freshwater stream of Fiji were analyzed. The consistently low Sr/Ca values (0–4) indicated upstream movement after settlement and freshwater or estuarine residence of all four individuals. These eels did not appear to have entered freshwater just for a short time period, which is consistent with other reports that this species is present in estuarine and freshwater habitats. This suggests that G. polyuranodon may be a catadromous species of marine eel. The similarities and differences between the life histories of anguillid eels and the few marine eels that have evolved the ability to invade freshwater habitats is discussed in relation to the evolutionary origin of diadromy in anguilliform fishes that originated in the marine environment.     

The evolution of diadromy in fishes (revisited) and its place in phylogenetic analysis

Diadromy is a term used to describe migrations of fishes between fresh waters and the sea; these migrations are regular, physiologically mediated movements which occur at predictable life history phases in each diadromous species, they involve most members of a species' populations, and they are usually obligatory. Around 250 fish species are regarded as diadromous. A review of the life history strategies amongst families of fishes that include diadromous species provides little support for a suggested scenario for their evolution that involves: (1) evolution of anadromy via amphidromy from fishes of marine origins, and (2) evolution of catadromy through amphidromy from fishes of freshwater origins, even though these scenarios seem intuitively reasonable. The various forms of diadromy appear to have had multiple independent origins amongst diverse fish groups. There is increasing confidence that behavioural characteristics of animals are heuristic in gener ating and interpreting phylogenies. However, examination of fishes shows wide variability of diadromous life histories within closely related families and genera, within species, and there is even ontogenetic variation in patterns of behaviour by individual fish. In addition, there is multiple loss of diadromy in many diadromous fish species in which the life history becomes restricted to fresh waters. This variation suggests that diadromy is a behavioural character of dubious worth in determining phylogenetic relationships. Moreover, it appears to have been an ancestral condition in some fish families, such as Anguillidae, Salmonidae, Galaxiidae, Osmeridae, and others, and perhaps in the whole salmonoid/osmeroid/galaxioid complex of families. This, too, makes diadromy of dubious worth in phylogenetic analysis     

Sweet or salty? The origin of freshwater gastrotrichs (Gastrotricha,Chaetonotida) revealed by molecular phylogenetic analysis

Chaetonotidae is the most diverse and widely distributed family of the order Chaetonotida (Gastrotricha) and includes both marine and freshwater species. Although the family is regarded as a sister taxon to the exclusively marine Xenotrichulidae, the type of environment, marine or freshwater, where Chaetonotidae originated is still not known. Here, we reconstructed the phylogeny of the family based on molecular sequence data and mapped both morphological and ecological characters to determine the ancestral environment of the first members of the family. Our results revealed that the freshwater genus Bifidochaetus is the earliest branching lineage in the paraphyletic Chaetonotidae (encompassing Dasydytidae and Neogosseidae). Moreover, we reconstructed Lepidochaetus-Cephalionotus clade as a monophyletic sister group to the remaining chaetonotids, which supports Kisielewski's morphological based hypothesis concerning undifferentiated type of body scales as a most primary character in Chaetonotidae. We also found that reversals to marine habitats occurred independently in different Chaetonotidae lineages, thus marine species in the genera Heterolepidoderma, Halichaetonotus, Aspidiophorus and subgenera Chaetonotus (Schizochaetonotus) or Chaetonotus (Marinochaetus) should be assumed as having secondarily invaded the marine environment. Character mapping revealed a series of synapomorphies that define the clade that includes Chaetonotidae (with Dasydytidae and Neogosseidae), the most important of which may be those linked to reproduction.     

Evolutionary origins and diversification of proteobacterial mutualists

Mutualistic bacteria infect most eukaryotic species in nearly every biome. Nonetheless, two dilemmas remain unresolved about bacterial–eukaryote mutualisms: how do mutualist phenotypes originate in bacterial lineages and to what degree do mutualists traits drive or hinder bacterial diversification? Here, we reconstructed the phylogeny of the hyperdiverse phylum Proteobacteria to investigate the origins and evolutionary diversification of mutualistic bacterial phenotypes. Our ancestral state reconstructions (ASRs) inferred a range of 34–39 independent origins of mutualist phenotypes in Proteobacteria, revealing the surprising frequency with which host-beneficial traits have evolved in this phylum. We found proteobacterial mutualists to be more often derived from parasitic than from free-living ancestors, consistent with the untested paradigm that bacterial mutualists most often evolve from pathogens. Strikingly, we inferred that mutualists exhibit a negative net diversification rate (speciation minus extinction), which suggests that mutualism evolves primarily via transitions from other states rather than diversification within mutualist taxa. Moreover, our ASRs infer that proteobacterial mutualist lineages exhibit a paucity of reversals to parasitism or to free-living status. This evolutionary conservatism of mutualism is contrary to long-standing theory, which predicts that selection should often favour mutants in microbial mutualist populations that exploit or abandon more slowly evolving eukaryotic hosts.     

Experimental adaptation to marine conditions by a freshwater alga

The marine‐freshwater boundary has been suggested as one of the most difficult to cross for organisms. Salt is a major ecological factor and provides an unequalled range of ecological opportunity because marine habitats are much more extensive than freshwater habitats, and because salt strongly affects the structure of microbial communities. We exposed experimental populations of the freshwater alga Chlamydomonas reinhardtii to steadily increasing concentrations of salt. About 98% of the lines went extinct. The ones that survived now thrive in growth medium with 36 g?L^?1 NaCl, and in seawater. Our results indicate that adaptation to marine conditions proceeded first through genetic assimilation of an inducible response to relatively low salt concentrations that was present in the ancestors, and subsequently by the evolution of an enhanced inducible response to high salt concentrations. These changes appear to have evolved through reversible and irreversible modifications, respectively. The evolution of marine from freshwater lineages is an example that clearly indicates the possibility of studying certain aspects of major ecological transitions in the laboratory.     

Sphaeriid and corbiculid clams represent separate heterodont bivalve radiations into freshwater environments

Nine families of bivalve molluscs have undergone successful radiations in freshwater habitats, including three heterodont taxa: the Sphaeriidae, Corbiculidae, and Dreissenidae. Although the phylogenetic relationships of these freshwater heterodont families are controversial, most workers place the first two in the superfamily Corbiculoidea and assume that they represent a monophyletic grouping. We have tested competing phylogenetic hypotheses for the Corbiculoidea by constructing a representative molecular phylogeny, based on domains D1-D3 of the nuclear large subunit 28S rDNA, for 18 heterodont bivalves and for two oyster outgroup taxa. Our results do not support the monophyly of the Corbiculoidea and are consistent with the hypothesis that all three families of freshwater heterodonts represent independent colonization events by marine ancestors. Similarities in developmental mode specializations exhibited by some sphaeriids and corbiculids, such as sequential direct-developing broods, represent convergent adaptations to the freshwater environment. The corbiculid taxa form a clade with venerid and mactrid outgroups but we were not able to identify a putative marine outgroup for the sphaeriids.     

Inferring the biogeographic origins of inter‐continental disjunct endemics using a Bayes‐DIVA approach

The arcto‐Tertiary relictual flora is comprised of many genera that occur non‐contiguously in the temperate zones of eastern Asia, Europe, eastern North America, and western North America. Within each distributional area, species are typically endemic and may thus be widely separated from closely related species within the other areas. It is widely accepted that this common pattern of distribution resulted from of the fragmentation of a once more‐continuous arcto‐Tertiary forest. The historical biogeographic events leading to the present‐day disjunction have often been investigated using a phylogenetic approach. Limitations to these previous studies have included phylogenetic uncertainty and uncertainty in ancestral range reconstructions. However, the recently described Bayes‐DIVA method handles both types of uncertainty. Thus, we used Bayes‐DIVA analysis to reconstruct the stem lineage distributions for 185 endemic lineages from 23 disjunct genera representing 17 vascular plant families. In particular, we asked whether endemic lineages within each of the four distributional areas more often evolved from (1) widespread ancestors, (2) ancestors dispersed from other areas, or (3) endemic ancestors. We also considered which of these three biogeographic mechanisms may best explain the origins of arcto‐Tertiary disjunct endemics in the neotropics. Our results show that eastern Asian endemics more often evolved from endemic ancestors compared to endemics in Europe and eastern and western North America. Present‐day endemic lineages in the latter areas more often arose from widespread ancestors. Our results also provide anecdotal evidence for the importance of dispersal in the biogeographic origins of arcto‐Tertiary species endemic in the neotropics.     

Searching factors causing implausible non-monophyly: ssu rDNA phylogeny of Isopoda Asellota (Crustacea: Peracarida) and faster evolution in marine than in freshwater habitats

This contribution addresses two questions: which alignment patterns are causing non-monophyly of the Asellota and what is the phylogenetic history of this group? The Asellota are small benthic crustaceans occurring in most aquatic habitats. In view of the complex morphological apomorphies known for this group, monophyly of the Asellota has never been questioned. Using ssu rDNA sequences of outgroups and of 16 asellote species from fresh water, littoral marine habitats and from deep-sea localities, the early divergence between the lineages in fresh water and in the ocean, and the monophyly of the deep-sea taxon Munnopsidae are confirmed. Relative substitution rates of freshwater species are much lower than in other isopod species, rates being highest in some littoral marine genera (Carpias and Jaera). Furthermore, more sequence sites are variable in marine than in freshwater species, the latter conserve outgroup character states. Monophyly is recovered with parsimony methods, but not with distance and maximum likelihood analyses, which tear apart the marine from the freshwater species. The information content of alignments was studied with spectra of supporting positions. The scarcity of signal (=apomorphic nucleotides) supporting monophyly of the Asellota is attributed to a short stem-line of this group or to erosion of signal in fast evolving marine species. Parametric boostrapping in combination with spectra indicates that a tree model cannot explain the data and that monophyly of the Asellota should not be rejected even though many topologies do not recover this taxon.     

Evolutionary bottlenecks in brackish water habitats drive the colonization of fresh water by stingrays

Species richness in freshwater bony fishes depends on two main processes: the transition into and the diversification within freshwater habitats. In contrast to bony fishes, only few cartilaginous fishes, mostly stingrays (Myliobatoidei), were able to colonize fresh water. Respective transition processes have been mainly assessed from a physiological and morphological perspective, indicating that the freshwater lifestyle is strongly limited by the ability to perform osmoregulatory adaptations. However, the transition history and the effect of physiological constraints on the diversification in stingrays remain poorly understood. Herein, we estimated the geographic pathways of freshwater colonization and inferred the mode of habitat transitions. Further, we assessed habitat‐related speciation rates in a time‐calibrated phylogenetic framework to understand factors driving the transition of stingrays into and the diversification within fresh water. Using South American and Southeast Asian freshwater taxa as model organisms, we found one independent freshwater colonization event by stingrays in South America and at least three in Southeast Asia. We revealed that vicariant processes most likely caused freshwater transition during the time of major marine incursions. The habitat transition rates indicate that brackish water species switch preferably back into marine than forth into freshwater habitats. Moreover, our results showed significantly lower diversification rates in brackish water lineages, whereas freshwater and marine lineages exhibit similar rates. Thus, brackish water habitats may have functioned as evolutionary bottlenecks for the colonization of fresh water by stingrays, probably because of the higher variability of environmental conditions in brackish water.