Host shifts in economically significant fruit flies (Diptera: Tephritidae) with high degree of polyphagy

Insects tend to feed on related hosts. Coevolution tends to be dominated by interactions resulting from plant chemistry in defense strategies, and evolution of secondary metabolisms being in response to insect herbivory remains a classic explanation of coevolution. The present study examines whether evolutionary constraints existing in host associations of economically important fruit flies in the species‐rich tribe Dacini (Diptera: Tephritidae) and to what extent these species have evolved specialized dietary patterns. We found a strong effect of host phylogeny on associations on the 37 fruit flies tested, although the fruit fly species feeding on ripe commercially grown fruits that lost the toxic compounds after long‐term domestication are mostly polyphagous. We assessed the phylogenetic signal of host breadth across the fruit fly species, showing that the results were substantially different depending on partition levels. Further, we mapped main host family associations onto the fruit fly phylogeny and Cucurbitaceae has been inferred as the most likely ancestral host family for Dacini based on ancestral state reconstruction.     

Reconstructing ancestral ranges in historical biogeography: properties and prospects

Recent years have witnessed a proliferation of quantitative methods for biogeographic inference. In particular, novel parametric approaches represent exciting new opportunities for the study of range evolution. Here, we review a selection of current methods for biogeographic analysis and discuss their respective properties. These methods include generalized parsimony approaches, weighted ancestral area analysis, dispersal-vicariance analysis, the dispersal--extinction--cladogenesis model and other maximum likelihood approaches, and Bayesian stochastic mapping of ancestral ranges, including a novel approach to inferring range evolution in the context of island biogeography. Some of these methods were developed specifically for problems of ancestral range reconstruction, whereas others were designed for more general problems of character state reconstruction and subsequently applied to the study of ancestral ranges. Methods for reconstructing ancestral history on a phylogenetic tree differ not only in the types of ancestral range states that are allowed, but also in the various historical events that may change the ancestral ranges. We explore how the form of allowed ancestral ranges and allowed transitions can both affect the outcome of ancestral range estimation. Finally, we mention some promising avenues for future work in the development of model-based approaches to biogeographic analysis.     

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.     

Phylogenetic distribution of compatible solute synthesis genes support a freshwater origin for cyanobacteria

Previous work using ancestral state reconstruction of habitat salinity preference proposed that the early cyanobacteria likely lived in a freshwater environment. The aim of this study was to test that hypothesis by performing phylogenetic analyses of the genes underlying salinity preferences in the cyanobacteria. Phylogenetic analysis of compatible solute genes shows that sucrose synthesis genes were likely ancestral in the cyanobacteria, and were also likely inherited during the cyanobacterial endosymbiosis and into the photosynthetic algae and land plants. In addition, the genes for the synthesis of compatible solutes that are necessary for survival in marine and hypersaline environments (such as glucosylglycerol, glucosylglycerate, and glycine betaine) were likely acquired independently high up (i.e., more recently) in the cyanobacterial tree. Because sucrose synthesis is strongly associated with growth in a low salinity environment, this independently supports a freshwater origin for the cyanobacteria. It is also consistent with geologic evidence showing that the early oceans were much warmer and saltier than modern oceans—sucrose synthesis alone would have been insufficient for early cyanobacteria to have colonized early Precambrian oceans that had a higher ionic strength. Indeed, the acquisition of an expanded set of new compatible solute genes may have enabled the historical colonization of marine and hypersaline environments by cyanobacteria, midway through their evolutionary history.     

Life in the arena: infaunal gastropods and the late Phanerozoic expansion of marine ecosystems into sand

Marine ecosystems have expanded into the infaunal realm below the surface of soft sediments throughout the Phanerozoic eon. During the Palaeozoic era, this expansion largely involved sedentary animals living in permanent resting places. Active sand‐burrowing animals colonized the infaunal environment later, but when this happened and when specialization for infaunal life evolved remain open questions. Here, phylogenetic evidence, fossil occurrences and previously established criteria for recognizing the sand‐burrowing habit in marine gastropods are used to determine how many gastropod clades became infaunal and when the transitions from surface‐dwelling to infaunal life occurred. At least 20, and as many as 35, clades (all but one of post‐Palaeozoic age) contain actively infaunal species. The overwhelming majority (15 of 20 clades) became infaunal during the Cenozoic, and clades with hundreds of infaunal species in the living fauna diversified beginning in the Early Miocene. The repeated evolution of, and specialization to, the sand‐burrowing habit by gastropods and other animals was enabled by increased habitat availability and higher marine productivity, and was necessitated by intensifying predation. As a result, the infaunal realm was transformed from a marine refuge to an integrated part of the marine biosphere in which high performance in locomotion and defence has become the norm.     

Robustness of ancestral state estimates: evolution of life history strategy in ichneumonoid parasitoids

We test hypotheses for the evolution of a life history trait among a group of parasitoid wasps (Hymenoptera: Ichneumonoidea), namely, the transition among koinobiont parasitoids (parasitoids whose hosts continue development after oviposition) between attacking exposed hosts and attacking hosts that are concealed within plant tissue. Using a range of phylogeny estimates based on 28S rDNA sequences, we use maximum parsimony (MP) and maximum likelihood (ML) methods to estimate the ancestral life history traits for the main clades in which both traits occur (using the programs MacClade and Discrete, respectively). We also assess the robustness of these estimates; for MP, we use step matrices in PAUP* to find the minimum weight necessary to reverse estimates or make them ambiguous, and for ML, we measure the differences in likelihood after fixing the ancestral nodes at the alternative states. We also measure the robustness of the MP ancestral state estimate against uncertainties in the phylogeny estimate, manipulating the most-parsimonious tree in MacClade to find the shortest suboptimal tree in which the ancestral state estimate is reversed or made ambiguous. Using these methods, we find strong evidence supporting two transitions among koinobiont Ichneumonoidea: (1) to attacking exposed hosts in a clade consisting of the Helconinae and related subfamilies, and (2) the reverse transition in a clade consisting of the Euphorinae and related subfamilies. In exploring different methods of analyzing variable-length DNA sequences, we found that direct optimization with POY gave some clearly erroneous results that had a profound effect on the overall phylogeny estimate. We also discuss relationships within the superfamily and expand the Mesostoinae to include all the gall-associated braconids that form the sister group of the Aphidiinae.     

Rapid maximum likelihood ancestral state reconstruction of continuous characters: A rerooting‐free algorithm

Ancestral state reconstruction is a method used to study the evolutionary trajectories of quantitative characters on phylogenies. Although efficient methods for univariate ancestral state reconstruction under a Brownian motion model have been described for at least 25 years, to date no generalization has been described to allow more complex evolutionary models, such as multivariate trait evolution, non‐Brownian models, missing data, and within‐species variation. Furthermore, even for simple univariate Brownian motion models, most phylogenetic comparative R packages compute ancestral states via inefficient tree rerooting and full tree traversals at each tree node, making ancestral state reconstruction extremely time‐consuming for large phylogenies. Here, a computationally efficient method for fast maximum likelihood ancestral state reconstruction of continuous characters is described. The algorithm has linear complexity relative to the number of species and outperforms the fastest existing R implementations by several orders of magnitude. The described algorithm is capable of performing ancestral state reconstruction on a 1,000,000‐species phylogeny in fewer than 2 s using a standard laptop, whereas the next fastest R implementation would take several days to complete. The method is generalizable to more complex evolutionary models, such as phylogenetic regression, within‐species variation, non‐Brownian evolutionary models, and multivariate trait evolution. Because this method enables fast repeated computations on phylogenies of virtually any size, implementation of the described algorithm can drastically alleviate the computational burden of many otherwise prohibitively time‐consuming tasks requiring reconstruction of ancestral states, such as phylogenetic imputation of missing data, bootstrapping procedures, Expectation‐Maximization algorithms, and Bayesian estimation. The described ancestral state reconstruction algorithm is implemented in the Rphylopars functions anc.recon and phylopars.     

Concatenated data and dense taxon sampling clarify phylogeny and ecological transitions within Hypotricha

Ciliates are single‐cell eukaryotes playing important roles in various ecosystems. Phylogenetic relationships within Hypotricha, one of the most polymorphic and highly derived ciliate groups, remain uncertain. Previous studies suggested that low genetic divergence might be the reason for poorly supported SSU rDNA tree topologies, despite the high morphological diversity of this group. In this study, we substantially increase the number of available hypotrich LSU rDNA gene sequences by the addition of 857 environmental sequences, and we investigate whether a more divergent gene and dense taxon sampling could better resolve the phylogeny of Hypotricha and shed light on the patterns of ecological transitions in the evolutionary history of the group. Pairwise distances of LSU rDNA sequences are generally higher than those for SSU rDNA within each order of Hypotricha, and both concatenated rDNA and LSU rDNA trees provide more resolution for hypotrich phylogenetics. Three traditional (morphology based) hypotrich orders, Stichotrichida, Sporadotrichida and Urostylida, are polyphyletic, but a monophyletic core Urostylida are found in our trees. A brackish/marine environment is inferred as ancestral within Hypotricha, with subsequent ecological diversification into freshwater, soil environments before the origin of major clades and some transitions back to the marine. However, inferred ecological transitions in Hypotricha are influenced by genes, methods and taxa.     

The mitochondrial phylogeny of an ancient lineage of ray-finned fishes (Polypteridae) with implications for the evolution of body elongation,pelvic fin loss,and craniofacial morphology in Osteichthyes

Background  

The family Polypteridae, commonly known as "bichirs", is a lineage that diverged early in the evolutionary history of Actinopterygii (ray-finned fish), but has been the subject of far less evolutionary study than other members of that clade. Uncovering patterns of morphological change within Polypteridae provides an important opportunity to evaluate if the mechanisms underlying morphological evolution are shared among actinoptyerygians, and in fact, perhaps the entire osteichthyan (bony fish and tetrapods) tree of life. However, the greatest impediment to elucidating these patterns is the lack of a well-resolved, highly-supported phylogenetic tree of Polypteridae. In fact, the interrelationships of polypterid species have never been subject to molecular phylogenetic analysis. Here, we infer the first molecular phylogeny of bichirs, including all 12 recognized species and multiple subspecies using Bayesian analyses of 16S and cyt-b mtDNA. We use this mitochondrial phylogeny, ancestral state reconstruction, and geometric morphometrics to test whether patterns of morphological evolution, including the evolution of body elongation, pelvic fin reduction, and craniofacial morphology, are shared throughout the osteichthyan tree of life.     

Inferring the ancestral sexuality and reproductive condition in sponges (Porifera)

Considerable diversity abounds among sponges with respect to reproductive and developmental biology. Their ancestral sexual mode (gonochorism vs. hermaphroditism) and reproductive condition (oviparity vs. viviparity) however remain unclear, and these traits appear to have undergone correlated evolution in the phylum. To infer ancestral traits and investigate this putative correlation, we used DNA sequence data from two loci (18S ribosomal RNA and cytochrome c oxidase subunit I) to explore the phylogenetic relationships of 62 sponges whose reproductive traits have been previously documented. Although the inferred tree topologies, using the limited data available, favoured paraphyly of sponges, we also investigated ancestral character‐state reconstruction on a phylogeny with constrained sponge monophyly. Both parsimony‐ and likelihood‐based ancestral state reconstructions indicate that viviparity (brooding) was the likely reproductive mode of the ancestral sponge. Hermaphroditism is favoured over gonochorism as the sexual condition of the sponge ancestor under parsimony, but the reconstruction is ambiguous under likelihood, rendering the ancestry of sexuality unresolved in our study. These results are insensitive to the constraint of sponge monophyly when tracing the reproductive characters using parsimony methods. However, the maximum likelihood analysis of the monophyletic hypothetical tree rendered gonochorism as ancestral for the phylum. A test of trait correlation unambiguously favours the concerted evolution of sexuality and reproductive mode in sponges (hermaphroditism/viviparity, gonochorism/oviparity). Although testing ecological hypotheses for the pattern of sponge reproduction is beyond the scope of our analyses, we postulate that certain physiological constrains might be key causes for the correlation of reproductive characters.     

Exact and heuristic algorithms for the Indel Maximum Likelihood Problem.

Given a multiple alignment of orthologous DNA sequences and a phylogenetic tree for these sequences, we investigate the problem of reconstructing the most likely scenario of insertions and deletions capable of explaining the gaps observed in the alignment. This problem, that we called the Indel Maximum Likelihood Problem (IMLP), is an important step toward the reconstruction of ancestral genomics sequences, and is important for studying evolutionary processes, genome function, adaptation and convergence. We solve the IMLP using a new type of tree hidden Markov model whose states correspond to single-base evolutionary scenarios and where transitions model dependencies between neighboring columns. The standard Viterbi and Forward-backward algorithms are optimized to produce the most likely ancestral reconstruction and to compute the level of confidence associated to specific regions of the reconstruction. A heuristic is presented to make the method practical for large data sets, while retaining an extremely high degree of accuracy. The methods are illustrated on a 1-Mb alignment of the CFTR regions from 12 mammals.     

Mitogenomes provide new insights of evolutionary history of Boreheptagyiini and Diamesini (Diptera: Chironomidae: Diamesinae)

Mitogenomes have been widely used for phylogenetic reconstruction of various Dipteran groups, but specifically for chironomid, they have not been carried out to resolve the relationships. Diamesinae (Diptera: Chironomidae) are important bioindicators for freshwater ecosystem monitoring, but its evolutionary history remains uncertain for lack of information. Here, coupled with one previously published and 30 new mitogenomes of Diamesinae, we carried out comparative mitogenomic analysis and phylogenetic analysis. Mitogenomes of Diamesinae were conserved in structure, and all genes arranged in the same order as the ancestral insect mitogenome. All protein‐coding genes in Diamesinae were under stronger purifying selection than those of other nonbiting midge species, which may exhibit signs of adaptation to life at cold living conditions. Phylogenetic analyses strongly supported the monophyly of Diamesinae, with Boreheptagyiini deeply nested within Diamesini. In addition, phylogenetic relationship of selected six genera was resolved, except Sympotthastia remained unstable. Our study revealed that the mitogenomes of Diamesinae are highly conserved, and they are practically useful for phylogenetic inference.     

GeneTRACE-reconstruction of gene content of ancestral species

While current computational methods allow the reconstruction of individual ancestral protein sequences, reconstruction of complete gene content of ancestral species is not yet an established task. In this paper, we describe GENETRACE, an efficient linear-time algorithm that allows the reconstruction of evolutionary history of individual protein families as well as the complete gene content of ancestral species. The performance of the method was validated with a simulated evolution program called SimulEv. Our results indicate that given a set of correct phylogenetic profiles and a correct species tree, ancestral gene content can be reconstructed with sensitivity and selectivity of more than 90%. SimulEv simulations were also used to evaluate performance of the reconstruction of gene content-based phylogenetic trees, suggesting that these trees may be accurate at the terminal branches but suffer from long branch attraction near the root of the tree.     

Recreated Ancestral Opsin Associated with Marine to Freshwater Croaker Invasion Reveals Kinetic and Spectral Adaptation

Rhodopsin, the light-sensitive visual pigment expressed in rod photoreceptors, is specialized for vision in dim-light environments. Aquatic environments are particularly challenging for vision due to the spectrally dependent attenuation of light, which can differ greatly in marine and freshwater systems. Among fish lineages that have successfully colonized freshwater habitats from ancestrally marine environments, croakers are known as highly visual benthic predators. In this study, we isolate rhodopsins from a diversity of freshwater and marine croakers and find that strong positive selection in rhodopsin is associated with a marine to freshwater transition in South American croakers. In order to determine if this is accompanied by significant shifts in visual abilities, we resurrected ancestral rhodopsin sequences and tested the experimental properties of ancestral pigments bracketing this transition using in vitro spectroscopic assays. We found the ancestral freshwater croaker rhodopsin is redshifted relative to its marine ancestor, with mutations that recapitulate ancestral amino acid changes along this transitional branch resulting in faster kinetics that are likely to be associated with more rapid dark adaptation. This could be advantageous in freshwater due to the redshifted spectrum and relatively narrow interface and frequent transitions between bright and dim-light environments. This study is the first to experimentally demonstrate that positively selected substitutions in ancestral visual pigments alter protein function to freshwater visual environments following a transition from an ancestrally marine state and provides insight into the molecular mechanisms underlying some of the physiological changes associated with this major habitat transition.     

Supertree analyses of the roles of viviparity and habitat in the evolution of atherinomorph fishes

Using supertree phylogenetic reconstructions, we investigate how livebearing and freshwater adaptations may have shaped evolutionary patterns in the Atherinomorpha, a large clade (approximately 1500 extant species) of ray-finned fishes. Based on maximum parsimony reconstructions, livebearing appears to have evolved at least four times independently in this group, and no reversions to the ancestral state of oviparity were evident. With respect to habitat, at least five evolutionary transitions apparently occurred from freshwater to marine environments, at least two transitions in the opposite direction, and no clear ancestral state was identifiable. All viviparous clades exhibited more extant species than their oviparous sister taxa, suggesting that transitions to viviparity may be associated with cladogenetic diversification. Transitions to freshwater were usually, but not invariably associated with increased species richness, but the trend was, overall, not significant among sister clades. Additionally, we investigated whether livebearing and freshwater adaptations are currently associated with elevated risks of extinction as implied by species' presence on the 2004 IUCN Red List. Despite being correlated with decreased brood size, livebearing has not significantly increased extinction risk in the Atherinomorpha. However, freshwater species were significantly more likely than marine species to be listed as endangered.     

On nitric oxide signaling,metamorphosis, and the evolution of biphasic life cycles

Summary Complex life cycles are ancient and widely distributed, particularly so in the marine environment. Generally, the marine biphasic life cycle consists of pre‐reproductive stages that exist in the plankton for various periods of time before settling and transforming into a benthic reproductive stage. Pre‐reproductive stages are frequently phenotypically distinct from the reproductive stage, and the life cycle transition (metamorphosis) linking the larval and juvenile stages varies in extent of change but is usually rapid. Selection of suitable adult sites apparently involves the capacity to retain the larval state after metamorphic competence is reached. Thus two perennial and related questions arise: How are environmentally dependent rapid transitions between two differentiated functional life history stages regulated (a physiological issue) and how does biphasy arise (a developmental issue)? Two species of solitary ascidian, a sea urchin and a gastropod, share a nitric oxide (NO)‐dependent signaling pathway as a repressive regulator of metamorphosis. NO also regulates life history transitions among several simple eukaryotes. We review the unique properties of inhibitory NO signaling and propose that (a) NO is an ancient and widely used regulator of biphasic life histories, (b) the evolution of biphasy in the metazoa involved repression of juvenile development, (c) functional reasons why NO‐based signaling is well suited as an inhibitory regulator of metamorphosis after competence is reached, and (d) signaling pathways that regulate metamorphosis of extant marine animals may have participated in the evolution of larvae.     

A multi-gene phylogeny of Cephalopoda supports convergent morphological evolution in association with multiple habitat shifts in the marine environment

ABSTRACT: BACKGROUND: The marine environment is comprised of numerous divergent organisms living under similar selective pressures, often resulting in the evolution of convergent structures such as the fusiform body shape of pelagic squids, fishes, and some marine mammals. However, little is known about the frequency of, and circumstances leading to, convergent evolution in the open ocean. Here, we present a comparative study of the molluscan class Cephalopoda, a marine group known to occupy habitats from the intertidal to the deep sea. Several lineages bear features that may coincide with a benthic or pelagic existence, making this a valuable group for testing hypotheses of correlated evolution. To test for convergence and correlation, we generate the most taxonomically comprehensive multi-gene phylogeny of cephalopods to date. We then create a character matrix of habitat type and morphological characters, which we use to infer ancestral character states and test for correlation between habitat and morphology. RESULTS: Our study utilizes a taxonomically well-sampled phylogeny to show convergent evolution in all six morphological characters we analyzed. Three of these characters also correlate with habitat. The presence of an autogenic photophore is correlated with a pelagic habitat, while the cornea and accessory nidamental gland correlate with a benthic lifestyle. Here, we present the first statistical tests for correlation between convergent traits and habitat in cephalopods to better understand the evolutionary history of characters that are adaptive in benthic or pelagic environments, respectively. DISCUSSION: Our study supports the hypothesis that habitat has influenced convergent evolution in the marine environment: benthic organisms tend to exhibit similar characteristics that confer protection from invasion by other benthic taxa, while pelagic organisms possess features that facilitate crypsis and communication in an environment lacking physical refuges. Features that have originated multiple times in distantly related lineages are likely adaptive for the organisms inhabiting a particular environment: studying the frequency and evolutionary history of such convergent characters can increase understanding of the underlying forces driving ecological and evolutionary transitions in the marine environment.     

Ancestral populations perform better in a novel environment: domestication of medfly populations from five global regions

Geographically isolated populations of a species may differ in several aspects of life-history, morphology, behavior, and genetic structure as a result of adaptation in ecologically diverse habitats. We used a global invasive species, the Mediterranean fruit fly to investigate, whether adaptation to a novel environment differs among geographically isolated populations that vary in major life history components such as life span and reproduction. We used wild populations from five global regions (Kenya, Hawaii, Guatemala, Portugal, and Greece). Adult demographic traits were monitored in F(2), F(5), F(7) and F(9) generations in captivity. Although domestication in constant laboratory conditions had a different effect on the mortality and reproductive rates of the different populations, a general trend of decreasing life span and age of first reproduction was observed for most medfly populations tested. However, taking into account longevity of both sexes, age-specific reproductive schedules, and average reproductive rates we found that the ancestral Kenyan population kept the above life history traits stable during domestication compared to the other populations tested. These findings provide important insights in the life-history evolution of this model species, and suggest that ancestral medfly populations perform better than the derived - invasive ones in a novel environment.     

Speciation in marine environments: Diving under the surface

Marine environments are inhabited by a broad representation of the tree of life, yet our understanding of speciation in marine ecosystems is extremely limited compared with terrestrial and freshwater environments. Developing a more comprehensive picture of speciation in marine environments requires that we 'dive under the surface' by studying a wider range of taxa and ecosystems is necessary for a more comprehensive picture of speciation. Although studying marine evolutionary processes is often challenging, recent technological advances in different fields, from maritime engineering to genomics, are making it increasingly possible to study speciation of marine life forms across diverse ecosystems and taxa. Motivated by recent research in the field, including the 14 contributions in this issue, we highlight and discuss six axes of research that we think will deepen our understanding of speciation in the marine realm: (a) study a broader range of marine environments and organisms; (b) identify the reproductive barriers driving speciation between marine taxa; (c) understand the role of different genomic architectures underlying reproductive isolation; (d) infer the evolutionary history of divergence using model‐based approaches; (e) study patterns of hybridization and introgression between marine taxa; and (f) implement highly interdisciplinary, collaborative research programmes. In outlining these goals, we hope to inspire researchers to continue filling this critical knowledge gap surrounding the origins of marine biodiversity.     

Salinity influences the distribution of marine snakes: implications for evolutionary transitions to marine life

Secondary transitions from terrestrial to marine life provide remarkable examples of evolutionary change. Although the maintenance of osmotic balance poses a major challenge to secondarily marine vertebrates, its potential role during evolutionary transitions has not been assessed. In the current study, we investigate the role of oceanic salinity as a proximate physiological challenge for snakes during the phylogenetic transition from the land to the sea. Large‐scale biogeographical analyses using the four extant lineages of marine snakes suggest that salinity constrains their current distribution, especially in groups thought to resemble early transitional forms between the land and the sea. Analyses at the species‐level suggest that a more efficient salt‐secreting gland allows a species to exploit more saline, and hence larger, oceanic areas. Salinity also emerged as the strongest predictor of sea snake richness. Snake species richness was negatively correlated with mean annual salinity, but positively correlated with monthly variation in salinity. We infer that all four independent transitions from terrestrial to marine life in snakes may have occurred in the Indonesian Basin, where salinity is low and seasonally variable. More generally, osmoregulatory challenges may have influenced the evolutionary history and ecological traits of other secondarily marine vertebrates (turtles, birds and mammals) and may affect the impact of climate change on marine vertebrates.