Amphibious fish: why do they leave water?

Summary Amphibious behaviour in fish has evolved separately many times since the first amphibious fishes, the rhipidistian crossopterygians, ventured onto land about 350 million years ago. This behaviour has resulted in the colonization and eventual domination by vertebrates of the terrestrial habitat. It is generally proposed that aquatic hypoxia, owing to metabolic oxygen consumption and organic decay, was the most important selective force in the evolution of air-breathing vertebrates (e.g. Randall et al., 1981). Modern amphibious fish species give an insight into the reasons for leaving and eventually abandoning the aquatic habitat. Amphibious fishes today leave the water for a variety of reasons associated with degradation of their aquatic habitat, or biotic factors within it.The possible causal factors which may elicit an emergence response are summarized in Fig. 1(a) and (b). Amphibious fish inhabiting closed systems, as typified by freshwater or intertidal pools, may leave water for any of the reasons detailed in Fig. 1(a). The relative importance of any one stimulus is likely to vary between different species. However, it is possible that in closed systems, adverse fluctuations in physico-chemical parameters will have a more important effect in eliciting amphibious behaviour than will biotic factors. In open systems, such as coastal waters or large freshwater bodies, effectively two routes of escape from adverse aquatic conditions are available to amphibious fish. They may move onto land, or alternatively they may move underwater to find better conditions. In such a system, where physico-chemical parameters remain relatively constant, abiotic factors are unlikely to have a significant influence on amphibious behaviour. The dominant stimulus in open systems is possibly the three-way interaction between predation, competition, and short-or long-term food availability (Fig. 1(b)).It is unlikely that any one of the factors discussed in this review will act alone in causing amphibious behaviour, and in this respect the available literature on fish leaving water is lacking. Much of it is fragmentary and partly anecdotal, and the limited amount of experimental work tends to concentrate on individual causal factors. There is evidently scope for detailed examination of emersion in a number of amphibious fishes, testing a matrix of environmental and biotic stimuli, in an attempt to determine in more detail the reasons for such behaviour.     

Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodon‐tidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time‐calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.     

Habitat transitions alter the adaptive landscape and shape phenotypic evolution in needlefishes (Belonidae)

Habitat occupancy can have a profound influence on macroevolutionary dynamics, and a switch in major habitat type may alter the evolutionary trajectory of a lineage. In this study, we investigate how evolutionary transitions between marine and freshwater habitats affect macroevolutionary adaptive landscapes, using needlefishes (Belonidae) as a model system. We examined the evolution of body shape and size in marine and freshwater needlefishes and tested for phenotypic change in response to transitions between habitats. Using micro‐computed tomographic (µCT) scanning and geometric morphometrics, we quantified body shape, size, and vertebral counts of 31 belonid species. We then examined the pattern and tempo of body shape and size evolution using phylogenetic comparative methods. Our results show that transitions from marine to freshwater habitats have altered the adaptive landscape for needlefishes and expanded morphospace relative to marine taxa. We provide further evidence that freshwater taxa attain reduced sizes either through dwarfism (as inferred from axial skeletal reduction) or through developmental truncation (as inferred from axial skeletal loss). We propose that transitions to freshwater habitats produce morphological novelty in response to novel prey resources and changes in locomotor demands. We find that repeated invasions of different habitats have prompted predictable changes in morphology.     

Evolution,ecology and physiology of amphibious killifishes (Cyprinodontiformes)

The order Cyprinodontiformes contains an exceptional diversity of amphibious taxa, including at least 34 species from six families. These cyprinodontiforms often inhabit intertidal or ephemeral habitats characterized by low dissolved oxygen or otherwise poor water quality, conditions that have been hypothesized to drive the evolution of terrestriality. Most of the amphibious species are found in the Rivulidae, Nothobranchiidae and Fundulidae. It is currently unclear whether the pattern of amphibiousness observed in the Cyprinodontiformes is the result of repeated, independent evolutions, or stems from an amphibious common ancestor. Amphibious cyprinodontiforms leave water for a variety of reasons: some species emerse only briefly, to escape predation or capture prey, while others occupy ephemeral habitats by living for months at a time out of water. Fishes able to tolerate months of emersion must maintain respiratory gas exchange, nitrogen excretion and water and salt balance, but to date knowledge of the mechanisms that facilitate homeostasis on land is largely restricted to model species. This review synthesizes the available literature describing amphibious lifestyles in cyprinodontiforms, compares the behavioural and physiological strategies used to exploit the terrestrial environment and suggests directions and ideas for future research.     

Host conservatism,geography, and elevation in the evolution of a Neotropical moth radiation

The origins of evolutionary radiations are often traced to the colonization of novel adaptive zones, including unoccupied habitats or unutilized resources. For herbivorous insects, the predominant mechanism of diversification is typically assumed to be a shift onto a novel lineage of host plants. However, other drivers of diversification are important in shaping evolutionary history, especially for groups residing in regions with complex geological histories. We evaluated the contributions of shifts in host plant clade, bioregion, and elevation to diversification in Eois (Lepidoptera: Geometridae), a hyper‐diverse genus of moths found throughout the Neotropics. Relationships among 107 taxa were reconstructed using one mitochondrial and two nuclear genes. In addition, we used a genotyping‐by‐sequencing approach to generate 4641 SNPs for 137 taxa. Both datasets yielded similar phylogenetic histories, with relationships structured by host plant clade, bioregion, and elevation. While diversification of basal lineages often coincided with host clade shifts, more recent speciation events were more typically associated with shifts across bioregions or elevational gradients. Overall, patterns of diversification in Eois are consistent with the perspective that shifts across multiple adaptive zones synergistically drive diversification in hyper‐diverse lineages.     

Amphibious adaptations in a newly recognized amphibious fish: Terrestrial locomotion and the influences of body size and temperature

Amphibious animals are adapted for both aquatic and terrestrial habitats. The conflicting requirements for dual habitats are perhaps most pronounced in the air‐breathing fishes, which represent an intermediate stage between the totally aquatic habitat and terrestrial colonization. A key requirement for amphibious fishes is terrestrial locomotion. The different densities and compositions of air and water impose constraints for efficient terrestrial locomotion that differ from those required for aquatic locomotion. I investigated terrestrial locomotion in a small South African fish, Galaxias ‘nebula’, by exposing 60 individual fish to air in specially designed raceways and quantifying movement type and occurrence as a function of availability of water, fish size and environmental temperature. Nebula showed a sustained undulating form of terrestrial locomotion characteristic of amphibious fishes and also a transient ballistic locomotion (jumps) typical of fully aquatic species. Terrestrial movement was influenced by fish size, with medium‐sized fish undertaking more jumps towards water, and fewer jumps away from water, than their smaller or larger conspecifics. In contrast, axial undulation was mainly influenced by temperature. However, there was no consistent pattern in temperature effects presumably because temperature is just one of a suit of environmental factors that may affect terrestrial locomotion. Nebula's amphibious adaptations allow it to cope with the unpredictability inherent in its natural environment.     

Body shape vs. colour associated initial divergence in the Telmatherina radiation in Lake Matano, Sulawesi, Indonesia

Highly polymorphic colouration patterns are often associated with sexual selection in fish and can be the initial cause of divergence among closely related taxa. Here we use genetic, body colour and geometric morphometric data collected on 118 fish from Lake Matano, Sulawesi, Indonesia to test if colouration is the initial cause of divergence in the radiating Telmatherina genus. Results reveal that all Telmatherina previously described in this system can be categorized into three mitochondrial lineages and that colouration is only weakly associated with early divergence. Clade-specific body shapes, however, likely adapted to microenvironments are key to the initial divergence in this system. Data also show that although colourations were not likely instrumental in seeding divergence in these fish, they appear to have developed in parallel within each clade. Our results are consistent with an emerging pattern repeated in many vertebrate radiations, whereby divergence by colouration or other display traits is preceded by specialization to environmental adaptive peaks.     

Estimating the species tree for Hawaiian Schiedea (Caryophyllaceae) from multiple loci in the presence of reticulate evolution

Schiedea (Caryophyllaceae) is a monophyletic genus of 34 species, all endemic to the Hawaiian Islands, that arose from a single colonization, providing one of the best examples of adaptive radiation in Hawai'i. Species utilize a range of habitats and exhibit a variety of growth forms and transitions in breeding systems from hermaphroditism toward dimorphism or autogamy. Our study included the most thorough sampling to date: 2-5 individuals per species and 4 independent genetic partitions: eight plastid and three low-copy nuclear loci (9217bps), allowing a three-locus BEST species tree. Despite incomplete resolution at the tips, our results support monophyly for each extant species. Gene trees revealed several clear cases of cytonuclear incongruence, likely created by interspecific introgression. Conflict occurs at the divergence of section Alphaschiedea as well as at the tips. Ages inferred from a BEAST analysis allow an original colonization onto either Nihoa or Kauaì and inform some aspects of inter-island migrations. We suggest that several hard polytomies on the species tree are biologically realistic, signifying either nearly simultaneous speciation or historical introgressive hybridization. Based on inferred node ages that exceed expected coalescent times, we propose that undetected nuclear introgression may play a larger role than incomplete lineage sorting in sections Schiedea and Mononeura.     

Natural selection on MHC IIβ in parapatric lake and stream stickleback: Balancing,divergent, both or neither?

Major histocompatibility complex (MHC) genes encode proteins that play a central role in vertebrates' adaptive immunity to parasites. MHC loci are among the most polymorphic in vertebrates' genomes, inspiring many studies to identify evolutionary processes driving MHC polymorphism within populations and divergence between populations. Leading hypotheses include balancing selection favouring rare alleles within populations, and spatially divergent selection. These hypotheses do not always produce diagnosably distinct predictions, causing many studies of MHC to yield inconsistent or ambiguous results. We suggest a novel strategy to distinguish balancing vs. divergent selection on MHC, taking advantage of natural admixture between parapatric populations. With divergent selection, individuals with immigrant alleles will be more infected and less fit because they are susceptible to novel parasites in their new habitat. With balancing selection, individuals with locally rare immigrant alleles will be more fit (less infected). We tested these contrasting predictions using three‐spine stickleback from three replicate pairs of parapatric lake and stream habitats. We found numerous positive and negative associations between particular MHC IIβ alleles and particular parasite taxa. A few allele–parasite comparisons supported balancing selection, and others supported divergent selection between habitats. But, there was no overall tendency for fish with immigrant MHC alleles to be more or less heavily infected. Instead, locally rare MHC alleles (not necessarily immigrants) were associated with heavier infections. Our results illustrate the complex relationship between MHC IIβ allelic variation and spatially varying multispecies parasite communities: different hypotheses may be concurrently true for different allele–parasite combinations.     

Predators shape distribution and promote diversification of morphological defenses in <Emphasis Type="Italic">Leucorrhinia</Emphasis>, Odonata

Predators strongly influence species assemblages and shape morphological defenses of prey. Interestingly, adaptations that constitute effective defenses against one type of predator may render the prey susceptible to other types of predators. Hence, prey may evolve different strategies to escape predation, which may facilitate adaptive radiation of prey organisms. Larvae of different species in the dragonfly genus Leucorrhinia have various morphological defenses. We studied the distribution of these larvae in relation to the presence of predatory fish. In addition, we examined the variation in morphological defenses within species with respect to the occurrence of fish. We found that well-defended species, those with more and longer spines, were more closely associated with habitats inhabited by predatory fish and that species with weakly developed morphological defenses were more abundant in habitats without fish. The species predominantly connected to lakes with or without fish, respectively, were not restricted to a single clade in the phylogeny of the genus. Our data is suggestive of phenotypic plasticity in morphological defense in three of the studied species since these species showed longer spines in lakes with fish. We suggest that adaptive phenotypic plasticity may have broadened the range of habitats accessible to Leucorrhinia. It may have facilitated colonization of new habitats with different types of predators, and ultimately, speciation through adaptive radiation.     

Phenotypic plasticity facilitates initial colonization of a novel environment

Phenotypic plasticity can allow organisms to respond to environmental changes by producing better matching phenotypes without any genetic change. Because of this, plasticity is predicted to be a major mechanism by which a population can survive the initial stage of colonizing a novel environment. We tested this prediction by challenging wild Drosophila melanogaster with increasingly extreme larval environments and then examining expression of alcohol dehydrogenase (ADH) and its relationship to larval survival in the first generation of encountering a novel environment. We found that most families responded in the adaptive direction of increased ADH activity in higher alcohol environments and families with higher plasticity were also more likely to survive in the highest alcohol environment. Thus, plasticity of ADH activity was positively selected in the most extreme environment and was a key trait influencing fitness. Furthermore, there was significant heritability of ADH plasticity that can allow plasticity to evolve in subsequent generations after initial colonization. The adaptive value of plasticity, however, was only evident in the most extreme environment and had little impact on fitness in less extreme environments. The results provide one of the first direct tests of the adaptive role of phenotypic plasticity in colonizing a novel environment.     

Unveiling commonalities in understudied habitats of boulder-reefs: life-history traits of the widespread invertebrate and algal inhabitants

Compared to stable reef habitats, dynamic boulder-reefs (commonly called boulder-fields when intertidal) host many habitat specialist species. Most occur underneath boulders where they are largely hidden from view; only limited research has assessed their life-histories despite their widespread importance for biological diversity. But some abundant under-boulder species likely structuring this system are habitat generalists widely researched elsewhere. Here we review this research, focusing on three widespread under-boulder sessile taxa: spirorbids, serpulids (tubeworms) and nongeniculate coralline algae, and three mobile taxa: sea urchins, chitons and crabs. Spirorbids have extensive reproductive/colonization capabilities but are readily out-competed. We thus characterize spirorbids as mostly early-successional, while serpulids often have greater competitiveness. Nongeniculate corallines occur underneath boulders where light reaches, although they can withstand low levels of that and most other resources. Such traits characterize nongeniculate corallines as late-successional. Thus, succession underneath boulders may shift deterministically from early tubeworms to late nongeniculate corallines. Habitat generalist sea urchin and chiton species often have strong inter-specific interactions in exposed habitats. Future experiments may find that under-boulder aggregations of these taxa, and also crabs, are impacting algal and invertebrate assemblages. These experiments will be required if dynamic boulder-reefs are to be as thoroughly understood as other benthic systems.     

Evolutionary shifts in habitat aridity predict evaporative water loss across squamate reptiles

Aridity is an important determinant of species distributions, shaping both ecological and evolutionary diversity. Lizards and snakes are often abundant in deserts, suggesting a high potential for adaptation or acclimation to arid habitats. However, phylogenetic evidence indicates that squamate diversity in deserts may be more strongly tied to speciation within arid habitats than to convergent evolution following repeated colonization from mesic habitats. To assess the frequency of evolutionary transitions in habitat aridity while simultaneously testing for associated changes in water‐balance physiology, we analyzed estimates of total evaporative water loss (EWL) for 120 squamate species inhabiting arid, semiarid, or mesic habitats. Phylogenetic reconstructions revealed that evolutionary transitions to and from semiarid habitats were much more common than those between arid and mesic extremes. Species from mesic habitats exhibited significantly higher EWL than those from arid habitats, while species from semiarid habitats had intermediate EWL. Phylogenetic comparative methods confirmed this association between habitat aridity and EWL despite phylogenetic signal in each. Thus, the historical colonization of arid habitats by squamates is repeatedly associated with adaptive changes in EWL. This physiological convergence, which may reflect both phenotypic plasticity and genetic adaptation, has likely contributed to the success of squamates in arid environments.     

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.     

Exceptionally poor land snail fauna of central Yakutia (NE Russia): climatic and habitat determinants of species richness

There is an ongoing debate on the causes of the latitudinal diversity gradient, but diversity decline towards high latitudes is poorly documented for many invertebrate taxa. Therefore, we sampled land snail assemblages at 79 sites and in various habitat types in central Yakutia, a region with extremely continental, cool and dry climate. We tested whether habitats lacking suitable shelters for winter survival harbour less species than those with vegetation cover that softens climatic extremes. Both local species diversity and regional species diversity were extremely low: 13 species were recorded in total with an average of 1.4 species per site. While the majority of grassland sites were without snails (26 of 34 sites), forest sites supported at least one snail species in most cases (38 of 45 sites). Within grasslands, snail occurrences were associated with a higher herb-layer biomass. Numbers of snail species correlated with the amount of available calcium only in forests, in which species accumulation towards more favourable habitats was possible due to softening of climate harshness. As minute snails are known to be effective passive dispersers and the study area was not glaciated during the last glacial stage, there was certainly enough time for colonization of all favourable habitats. Our results suggest climatically driven limitations of both local and regional land snail diversity in central Yakutia. We conclude that the hypothesis of climate harshness remains the most probable explanation of a sharp drop in land snail diversity in high-latitude areas with cold climate.     

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.     

Evolution, insular restriction, and extinction of oceanic land crabs, exemplified by the loss of an endemic Geograpsus in the Hawaiian Islands

Most oceanic islands harbor unusual and vulnerable biotas as a result of isolation. As many groups, including dominant competitors and predators, have not naturally reached remote islands, others were less constrained to evolve novel adaptations and invade adaptive zones occupied by other taxa on continents. Land crabs are an excellent example of such ecological release, and some crab lineages made the macro-evolutionary transition from sea to land on islands. Numerous land crabs are restricted to, although widespread among, oceanic islands, where they can be keystone species in coastal forests, occupying guilds filled by vertebrates on continents. In the remote Hawaiian Islands, land crabs are strikingly absent. Here we show that absence of land crabs in the Hawaiian Islands is the result of extinction, rather than dispersal limitation. Analysis of fossil remains from all major islands show that an endemic Geograpsus was abundant before human colonization, grew larger than any congener, and extended further inland and to higher elevation than other land crabs in Oceania. Land crabs are major predators of nesting sea birds, invertebrates and plants, affect seed dispersal, control litter decomposition, and are important in nutrient cycling; their removal can lead to large-scale shifts in ecological communities. Although the importance of land crabs is obvious on remote and relatively undisturbed islands, it is less apparent on others, likely because they are decimated by humans and introduced biota. The loss of Geograpsus and potentially other land crabs likely had profound consequences for Hawaiian ecosystems.     

Transitions between marine and freshwater environments provide new clues about the origins of multicellular plants and algae

Marine–freshwater and freshwater–marine transitions have been key events in the evolution of life, and most major groups of organisms have independently undergone such events at least once in their history. Here, we first compile an inventory of bidirectional freshwater and marine transitions in multicellular photosynthetic eukaryotes. While green and red algae have mastered multiple transitions in both directions, brown algae have colonized freshwater on a maximum of six known occasions, and angiosperms have made the transition to marine environments only two or three times. Next, we review the early evolutionary events leading to the colonization of current habitats. It is commonly assumed that the conquest of land proceeded in a sequence from marine to freshwater habitats. However, recent evidence suggests that early photosynthetic eukaryotes may have arisen in subaerial or freshwater environments and only later colonized marine environments as hypersaline oceans were diluted to the contemporary level. Although this hypothesis remains speculative, it is important to keep these alternative scenarios in mind when interpreting the current habitat distribution of plants and algae. Finally, we discuss the roles of structural and functional adaptations of the cell wall, reactive oxygen species scavengers, osmoregulation, and reproduction. These are central for acclimatization to freshwater or to marine environments. We observe that successful transitions appear to have occurred more frequently in morphologically simple forms and conclude that, in addition to physiological studies of euryhaline species, comparative studies of closely related species fully adapted to one or the other environment are necessary to better understand the adaptive processes.     

Two waves of colonization straddling the K–Pg boundary formed the modern reef fish fauna

Living reef fishes are one of the most diverse vertebrate assemblages on Earth. Despite its prominence and ecological importance, the origins and assembly of the reef fish fauna is poorly described. A patchy fossil record suggests that the major colonization of reef habitats must have occurred in the Late Cretaceous and early Palaeogene, with the earliest known modern fossil coral reef fish assemblage dated to 50 Ma. Using a phylogenetic approach, we analysed the early evolutionary dynamics of modern reef fishes. We find that reef lineages successively colonized reef habitats throughout the Late Cretaceous and early Palaeogene. Two waves of invasion were accompanied by increasing morphological convergence: one in the Late Cretaceous from 90 to 72 Ma and the other immediately following the end-Cretaceous mass extinction. The surge in reef invasions after the Cretaceous–Palaeogene boundary continued for 10 Myr, after which the pace of transitions to reef habitats slowed. Combined, these patterns match a classic niche-filling scenario: early transitions to reefs were made rapidly by morphologically distinct lineages and were followed by a decrease in the rate of invasions and eventual saturation of morphospace. Major alterations in reef composition, distribution and abundance, along with shifts in climate and oceanic currents, occurred during the Late Cretaceous and early Palaeogene interval. A causal mechanism between these changes and concurrent episodes of reef invasion remains obscure, but what is clear is that the broad framework of the modern reef fish fauna was in place within 10 Myr of the end-Cretaceous extinction.