Freshwater Colonization Research Articles

GLOBAL ANALYSIS OF GENES INVOLVED IN FRESHWATER ADAPTATION IN THREESPINE STICKLEBACKS (GASTEROSTEUS ACULEATUS)

Examples of parallel evolution of phenotypic traits have been repeatedly demonstrated in threespine sticklebacks (Gasterosteus aculeatus) across their global distribution. Using these as a model, we performed a targeted genome scan--focusing on physiologically important genes potentially related to freshwater adaptation--to identify genetic signatures of parallel physiological evolution on a global scale. To this end, 50 microsatellite loci, including 26 loci within or close to (<6 kb) physiologically important genes, were screened in paired marine and freshwater populations from six locations across the Northern Hemisphere. Signatures of directional selection were detected in 24 loci, including 17 physiologically important genes, in at least one location. Although no loci showed consistent signatures of selection in all divergent population pairs, several outliers were common in multiple locations. In particular, seven physiologically important genes, as well as reference ectodysplasin gene (EDA), showed signatures of selection in three or more locations. Hence, although these results give some evidence for consistent parallel molecular evolution in response to freshwater colonization, they suggest that different evolutionary pathways may underlie physiological adaptation to freshwater habitats within the global distribution of the threespine stickleback.

CRYPTIC GENETIC VARIATION AND BODY SIZE EVOLUTION IN THREESPINE STICKLEBACK

The role of environment as a selective agent is well-established. Environment might also influence evolution by altering the expression of genetic variation associated with phenotypes under selection. Far less is known about this phenomenon, particularly its contribution to evolution in novel environments. We investigated how environment affected the evolvability of body size in the threespine stickleback (Gasterosteus aculeatus). Gasterosteus aculeatus is well suited to addressing this question due to the rapid evolution of smaller size in the numerous freshwater populations established following the colonization of new freshwater habitats by an oceanic ancestor. The repeated, rapid evolution of size following colonization contrasts with the general observation of low phenotypic variation in oceanic stickleback. We reared an oceanic population of stickleback under high and low salinity conditions, mimicking a key component of the ancestral environment, and freshwater colonization, respectively. There was low genetic variation for body size under high salinity, but this variance increased significantly when fish were reared under low salinity. We therefore conclude that oceanic populations harbor the standing genetic variation necessary for the evolution of body size, but that this variation only becomes available to selection upon colonization of a new habitat.

Natural selection and the genetics of adaptation in threespine stickleback

Growing knowledge of the molecular basis of adaptation in wild populations is expanding the study of natural selection. We summarize ongoing efforts to infer three aspects of natural selection--mechanism, form and history--from the genetics of adaptive evolution in threespine stickleback that colonized freshwater after the last ice age. We tested a mechanism of selection for reduced bony armour in freshwater by tracking genotype and allele frequency changes at an underlying major locus (Ectodysplasin) in transplanted stickleback populations. We inferred disruptive selection on genotypes at the same locus in a population polymorphic for bony armour. Finally, we compared the distribution of phenotypic effect sizes of genes underlying changes in body shape with that predicted by models of adaptive peak shifts following colonization of freshwater. Studies of the effects of selection on genes complement efforts to identify the molecular basis of adaptive differences, and improve our understanding of phenotypic evolution.

Colonization of Asian freshwaters by the Mytilidae (Bivalvia): a comparison of Sinomytilus harmandi from the Tonle-Sap River, Phnom Penh, Cambodia, with Limnoperna fortunei

Sinomytilus harmandi occurs in the lakes and rivers of Indochina, notably in Cambodia, Laos, Thailand and Vietnam and, again notably, the Mekong River and its myriad tributaries. Hitherto, this species and its four junior synonyms have been examined only superficially. Because of an interior shell septum, S. harmandi was originally assigned to the Dreissenidae (Bivalvia: Heterodonta), an anatomically distinct family naturally restricted to Europe and the Americas. In addition to S. harmandi, a secondspecies of mytilid mussel, Limnoperna fortunei, also occurs in Asian freshwater systems and both belong to the Mytilidae (Pteriomorphia), as demonstrated in this study for S. harmandi and elsewhere for L. fortunei. Sinomytilus harmandi is likely endemic to the Mekong River where it is sympatric with L. fortunei, the latter species being widely distributed in Indochina, south of and including the Yangtse River in China. Limnoperna fortunei is a highly opportunistic species that has been introduced into many locations outside its mainland Chinese borders, for example, Japan, Taiwan and South America. We suggest the possibility that L. fortunei has also been introduced into tropical Indochina from China. Because L. fortunei has a Devonian (~345-395 mya) modioline ancestry and S. harmandi is derived from a Permo-Trias (~265–225 mya) ancient mytiline ancestor it appears that Asian freshwater systems have been colonized by representatives of the Mytilidae on two separate temporal occasions.

Molecular phylogenetics supports multiple evolutionary transitions from marine to freshwater habitats in ariid catfishes

Transitions between the marine and freshwater environments represent an extraordinary ecological shift that has promoted diversification in many groups of aquatic organisms. Here, molecular phylogenetics is utilized to investigate habitat transitions in a group of catfishes (Ariidae) that includes species inhabiting marine and brackish waters (>110 species) as well as freshwater environments (∼40 species). The Ariidae is nested within the Otophysi, the largest clade of primary freshwater fishes with four orders and 67 families. Optimizations of habitat transitions (freshwater vs. marine) onto a previously inferred phylogeny suggest a single invasion of marine waters at the root of the ariid tree followed by 10–15 events of freshwater colonization, implying reversion to the primitive otophysan condition. Thus, ariids provide an extraordinary example of bidirectional habitat transitions in fishes. Freshwater recolonization has occurred in all major provinces where ariids are present, such as the New World (Mesoamerica and South America), Madagascar, Africa, Southeast Asia, and the Sahul continent (Australia and New Guinea). The remarkable diversity of freshwater ariids in Australia–New Guinea and Mesoamerica is presumed to have been facilitated by the originally depauperate freshwater ichthyofaunas in both regions, particularly the low diversity of primary otophysan families in Mesoamerica and their absence in Australia and New Guinea. The lack of phylogenetic resolution among basal Sahul lineages coupled with their extraordinary level of morphological divergence and trophic diversity suggests an ancient rapid radiation promoted by freshwater colonization. For this reason, Sahul ariids represent an excellent system for studying diversification associated with habitat transitions.

Should I stay or should I go? TheEctodysplasinlocus is associated with behavioural differences in threespine stickleback

Adaptive divergence may be facilitated if morphological and behavioural traits associated with local adaptation share the same genetic basis. It is therefore important to determine whether genes underlying adaptive morphological traits are associated with variation in behaviour in natural populations. Positive selection on low-armour alleles at the Ectodysplasin (Eda) locus in threespine stickleback has led to the repeated evolution of reduced armour, following freshwater colonization by fully armoured marine sticklebacks. This adaptive divergence in armour between marine and freshwater populations would be facilitated if the low allele conferred a behavioural preference for freshwater environments. We experimentally tested whether the low allele is associated with preference for freshwater by measuring the preference of each Eda genotype for freshwater versus saltwater after acclimation to either salinity. We found no association between the Eda low allele and preference for freshwater. Instead, the low allele was significantly associated with a reduced preference for the acclimation environment. This behaviour may facilitate the colonization of freshwater habitats from the sea, but could also hinder local adaptation by promoting migration of low alleles between marine and freshwater environments.

ENVIRONMENT SPECIFIC PLEIOTROPY FACILITATES DIVERGENCE AT THEECTODYSPLASINLOCUS IN THREESPINE STICKLEBACK

Adaptive radiation occurs when divergent natural selection in different environments leads to phenotypic differentiation. The pleiotropic effects of underlying genes can either promote or constrain this diversification. Identifying the pleiotropic effects of genes responsible for divergent traits, and testing how the environment influences these effects, can therefore help to provide an understanding of how ecology drives evolutionary change between populations. Positive selection on low-armor alleles at the Ectodysplasin (Eda) locus in threespine stickleback has led to the repeated evolution of reduced armor in populations following freshwater colonization by fully armored marine sticklebacks. Here, we demonstrate that Eda has environmentally determined pleiotropic effects on armor and growth. When raised in freshwater, reduced armor sticklebacks carrying "low" alleles at Eda had increased growth rate relative to fully armored sticklebacks carrying "complete" alleles. In saltwater treatments this growth advantage was present during juvenile growth but lost during adult growth, suggesting that in this environment stickleback are able to develop full armor plates without sacrificing overall growth rate. The environment specific pleiotropic effects of Eda demonstrate that ecological factors can mediate the influence of genetic architecture in driving phenotypic evolution. Furthermore, because size is important for mate choice in stickleback, the growth rate differences influenced by Eda may have effects on reproductive isolation between marine and freshwater populations.

Environmental determinism of year‐to‐year recruitment variability of European eel Anguilla anguilla in a small coastal catchment, the Frémur River, north‐west France

The influence of environmental factors (mainly the river flow) on the year-to-year variability of European eel Anguilla anguilla fluvial recruitment in a small coastal catchment, the Frémur River (north-west France) was examined. A comprehensive survey of catches from fixed traps at two weirs located at 4.5 km (Pont es Omnes Dam) and 6.0 km (Bois Joli Dam) above the river mouth was carried out between 1997 and 2004. Young pigmented elvers (mean +/-s.d. total length, 133.7 +/- 29.6 mm) were recruited in eel-passes from February to October, but the main runs followed a modal curve from April to September with a peak centred in May to June. Catches varied greatly between years, from 381 to 26 765 elvers. For each trap, a positive linear relationship between monthly mean river flow that preceded the maximal intensity of captures and annual total catches was observed. These relationships explained 73.1% (P < 0.01) and 89.0% (P < 0.001) of the year-to-year variability of the recruitment observed in the Pont es Omnes and Bois Joli traps respectively. A significant increase in river flow at the beginning of the migration peak would thus trigger a greater proportion of A. anguilla settled in the estuary and in the downstream zone of the Fremur River to begin their freshwater colonization. The physicochemical roles of changes in river discharge in stimulating upstream migration are discussed. It is concluded that fluvial recruitment in the Fremur River is mainly determined by environmental factors.

From sea to land and beyond – New insights into the evolution of euthyneuran Gastropoda (Mollusca)

BackgroundThe Euthyneura are considered to be the most successful and diverse group of Gastropoda. Phylogenetically, they are riven with controversy. Previous morphology-based phylogenetic studies have been greatly hampered by rampant parallelism in morphological characters or by incomplete taxon sampling. Based on sequences of nuclear 18S rRNA and 28S rRNA as well as mitochondrial 16S rRNA and COI DNA from 56 taxa, we reconstructed the phylogeny of Euthyneura utilising Maximum Likelihood and Bayesian inference methods. The evolution of colonization of freshwater and terrestrial habitats by pulmonate Euthyneura, considered crucial in the evolution of this group of Gastropoda, is reconstructed with Bayesian approaches.ResultsWe found several well supported clades within Euthyneura, however, we could not confirm the traditional classification, since Pulmonata are paraphyletic and Opistobranchia are either polyphyletic or paraphyletic with several clades clearly distinguishable. Sacoglossa appear separately from the rest of the Opisthobranchia as sister taxon to basal Pulmonata. Within Pulmonata, Basommatophora are paraphyletic and Hygrophila and Eupulmonata form monophyletic clades. Pyramidelloidea are placed within Euthyneura rendering the Euthyneura paraphyletic.ConclusionBased on the current phylogeny, it can be proposed for the first time that invasion of freshwater by Pulmonata is a unique evolutionary event and has taken place directly from the marine environment via an aquatic pathway. The origin of colonisation of terrestrial habitats is seeded in marginal zones and has probably occurred via estuaries or semi-terrestrial habitats such as mangroves.

Global diversity of free living flatworms (Platyhelminthes, “Turbellaria”) in freshwater

This contribution reviews diversity of turbellarian species by biogeographical regions, with comments on species biology. The review draws on the database available at http://www.devbio.umesci.maine.edu/styler/turbellaria. Comparisons between regions suggest that species richness may be at least one order of magnitude higher than the currently reported number of species. In the context of the recent reconstructions of phylogeny of Platyhelminthes based on molecular data, the paper allows inferences as to the history of colonization of freshwaters by turbellarians. Specifically, four, or perhaps six, major invasions of freshwater habitats may have occurred in the Pangean period, each of which gave rise to a monophyletic freshwater taxon. In addition, several occasional invasions by representatives of marine taxa must have taken place.

Parasites, fossils and geologic history: Historical biogeography of the South American freshwater croakers, Plagioscion spp. (Teleostei, Sciaenidae)

A hypothesis on the historical biogeography of the freshwater croakers, Plagioscion spp. (Teleostei: Sciaenidae), is developed based on data from the phylogeny of their monogenoidean parasites (Platyhelminthes), the geology of South America and the fossil record. Analyses suggest that the common ancestor of Plagioscion spp. colonized freshwater concomitantly with the common ancestor of their parasites, Euryhaliotrema spp. Colonization probably occurred via a marine transgression through western Venezuela that developed about 20 million years ago (Mya). This transgression with its postulated highly variable temporal and spatial salinity conditions most likely represented the facilitating event associated with freshwater colonization. A less likely alternative, that colonization occurred via the Mar del Plata in southern South America, is not supported by the geographical distributions and putative phylogeny of extant species of Plagioscion.

Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus.

Historical contingency and determinism are often cast as opposing paradigms under which evolutionary diversification operates. It may be, however, that both factors act together to promote evolutionary divergence, although there are few examples of such interaction in nature. We tested phylogenetic predictions of an explicit historical model of divergence (double invasions of freshwater by marine ancestors) in sympatric species of three-spined sticklebacks (Gasterosteus aculeatus) where determinism has been implicated as an important factor driving evolutionary novelty. Microsatellite DNA variation at six loci revealed relatively low genetic variation in freshwater populations, supporting the hypothesis that they were derived by colonization of freshwater by more diverse marine ancestors. Phylogenetic and genetic distance analyses suggested that pairs of sympatric species have evolved multiple times, further implicating determinism as a factor in speciation. Our data also supported predictions based on the hypothesis that the evolution of sympatric species was contingent upon 'double invasions' of postglacial lakes by ancestral marine sticklebacks. Sympatric sticklebacks, therefore, provide an example of adaptive radiation by determinism contingent upon historical conditions promoting unique ecological interactions, and illustrate how contingency and determinism may interact to generate geographical variation in species diversity

Variations in body size of individuals at sexual maturity among local populations of the freshwater prawn Macrobrachium nipponense (de Haan), with special reference to freshwater colonization

Variations in body size of individuals at sexual maturity among local populations of the freshwater prawn Macrobrachium nipponense (de Haan), with special reference to freshwater colonization

Cytogenetic study of two species of needlefish (Belonidae) from Argentina

The chromosomes of the two species of needlefish, Potamorraphis cf. eigenmanni and Strongylura microps, from fresh waters of Argentina were analyzed using C‐banding and silver staining and their karyotypes were described for the first time. The former species possessed 2n‐54 and karyotype composed of three pairs metacentric to submetacentric chromosomes and 24 pairs of subtelo to telocentric chromosomes. The NORs were situated on the end of the shorter arms of one middle‐sized bi‐armed pair of chromosomes. The later species possessed 2n=50 and karyotype composed exclusively of subtelo to telocentric chromosomes gradually decreasing in size. The NORs were situated inter‐stitially on the third pair of chromosomes. One or two supernumerary chromosomes were observed in one individual of the sample. Present data indicate greater cytotaxonomic diversity among species of needlefish which might be associated with their colonization of fresh waters.

CLUTCH SIZE AND EGG SIZE IN FREE-LIVING AND PARASITIC COPEPODS: A COMPARATIVE ANALYSIS.

The evolution of reproductive strategies and the trade-off between number and size of eggs were investigated in a comparative analysis of free-living and parasitic copepods. Data from 1038 copepod species were used to obtain family averages for 105 families; the phylogenetic relationships among these families include 94 branching events or 94 independent contrasts on which the analysis was based. Transition from a free-living existence to parasitism on invertebrates resulted in small increases in body size. Transition from parasitism on invertebrates to parasitism on fish was associated with greater increases in body size. After controlling for body size, a switch to fish hosts resulted in an increase in the number of eggs produced and a reduction in egg size. Among all contrasts, there was a negative relationship between changes in relative clutch size and changes in relative egg size, suggesting the existence of a trade-off between egg size and numbers. However, opposite changes in these measures of clutch size and egg size were not quite more frequent than expected by chance, therefore indicating that investments into egg numbers are not necessarily made at the expense of egg size, and vice versa. Latitude affected copepod body size, clutch size, and egg size, whereas the effects of freshwater colonization or size of the fish host were not significant. Comparative analyses at either the genus or species levels within given taxa of copepods parasitic on fish provided limited support for a trade-off between clutch size and egg size, but were hampered by the small number of independent phylogenetic contrasts available. From the family-level comparative analysis, it appears that the evolutionary transition from a free life to parasitism on invertebrates, and the transition from parasitism on invertebrates to parasitism on fish, have led to changes in life-history traits in response to the different selective pressures associated with the different modes of life.

UNDERSTANDING THE EVOLUTION OF BEHAVIOR IN THREESPINE STICKLEBACK: THE VALUE OF GEOGRAPHIC VARIATION

AbstractThe endemic radiation of the threespine stickleback in North America possesses features that will permit us to gain unique insights into evolutionary pattern and process. Already, comparison of populations has demonstrated a remarkable level of adaptive differentiation in reproductive behavior across populations in both southern British Columbia, Canada, and the Cook Inlet Region of Alaska, U.S.A. In small, shallow lakes, threespine stickleback feed predominantly on benthic invertebrates in the shallow littoral zone. They form large groups that attack nests defended by males, and consume all of the young within. In contrast, in larger, more oligotrophic lakes, adult stickleback feed primarily on plankton in large open-water foraging groups. They do not form groups that cannibalize young in nests. In these non-cannibalistic populations, males perform more conspicuous courtship behavior than do those in cannibalistic populations, apparently because risk of attack by visually hunting conspecifics is low. Courtship in these lakes more often includes the conspicuous zig-zag dance, and less often, meandering and dorsal pricking. Anadromous populations tend to be cannibalistic, but also are often behaviorally intermediate. They incorporate the zig-zag dance in courtship more often than do males in cannibalistic freshwater populations, but also usually incorporate the less conspicuous dorsal pricking behavior. These results suggest that the ancestral condition was intermediate and that both cannibalistic and non-cannibalistic freshwater populations display some derived elements in their reproductive repertoires. This kind of comparison among populations thought to have been independently derived from the marine form can provide insights into the patterns and causes of adaptive diversification. For populations such as these, carefully chosen from disparate geographic locations so as to preclude common evolutionary history after colonization of freshwater,

Sphaeromatid lsopods (Crustacea) from Brackish Waters in Queensland, Australia

Exosphaeroides fluvialis gen. et sp.n. is recorded from a number of estuaries along the mainland coast of Queensland and Cymodetta gracilipes sp.n. is recorded from sediment amongst mangroves and in a ‘dry’ location on Lizard Island, in the Great Barrier Reef. The brackish water species Cymodetta gambosa Bowman &amp; Kühne is redescribed and the genus is transferred from the hemibranchiate to the platybranchiate group of Sphaeromatidae. Another brackish water sphaeromatid, Exosphaeroma alatum Baker, is also redescribed and is removed from the hemibranchiate Sphaeromatidae to form the type‐species of a eubranchiate genus, Ptyosphaera gen.n. Details are given of the occurrence of sphaeromatid isopods in brackish water in Australia. Sphaeroma triste Heller, a wood‐boring sphaeromatid, is reported from Australia for the first time. A discussion is given concerning the colonization of brackish water and freshwater by sphaeromatids throughout the world.

Influence of salinity on the eggs and larvae of the California killifish Fundulus parvipinnis

Effects of salinity on embryonic development and survival were determined for eggs and larvae of the California killifish Fundulus parvipinnis Girard. Incubation salinities over the range of 5 to 14‰ S produced the shortest incubation period, maximum yolk-conversion efficiency, largest larval size at hatching, and maximum viable hatch. Various morphometric measurements of the newly-hatched larvae were influenced significantly by incubation salinity. Fertilization salinity also effected certain development criteria; in general, lower fertilization salinities resulted in shorter incubation periods and larger larvae at hatching. A salinity range of 5 to 14 ‰ S is anggested as a physiological optimum, and the known freshwater affinity of the species suggests that an eventual freshwater colonization by the California killifish is possible.

Observations sur la faune aquatique souterraine de Cuba

A short account on some achievements of the cubano-romanian biospeleological expeditions to Cuba in the study of the aquatic subterranean faunas. The following divisions of the aquatic subterranean realm are reviewed together with their most characteristic faunal elements: “guano pools” and rimstone pools in the vadose zone of the caves; underground streams; water table (and other) lakes in the caves; “pozzos” carved in the limestone, and “grietas” which are vertical clefts in the limestone of marine terraces, giving access to fresh- or to brackish water; the interstitial of the marine beaches; the underflow of running waters. At present, thorough biospeleological research is being carried out almost everywhere in Central America; Cuba, which remained until recently rather poorly investigated, proves to be one of the most remarkable areas from this point of view. A few of the most interesting problems rose in the course of the study of the underground aquatic fauna of Cuba are listed. An interesting biogeographical problem is the following: some of the subterranean aquatic elements prove to be related to elements belonging to the fauna of the other Antilles and of Mexico, but not to the South-American fauna (as is the case for some terrestrial groups). The research undertaken will be a contribution to the problem of the divisions of the aquatic subterranean realm and of their reciprocal relations, in a warm and humid climate; it will also contribute an answer to the problem of the differences between temperate and tropical cave communities; finally, it allows one to perceive in its very progress the process of colonization of the subterranean freshwaters by elements of marine origin, either through the interstitial realm or through the fissures of the littoral limestones.

Colonization of fresh waters in the Republic of South Africa by Lymnaea columella Say (Mollusca: Gastropoda).

Lymnaea (Pseudosuccinea) columella Say 1817, described from specimens probably obtained in the vicinity of Philadelphia1, is widely distributed in still and slow-flowing waters in the eastern United States of America, Mexico, Central America, Cuba and the northern and central regions of South America1,2. Fossil specimens are known from the Pleistocene of North America, and another species of the sub-genus has been described from the Pliocene of the same region3. L. columella is believed to have been introduced by human agency, probably with aquatic plants, into Puerto Rico, Tenerife, South Africa and many European countries4.