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

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

Fossil‐based comparative analyses reveal ancient marine ancestry erased by extinction in ray‐finned fishes

The marine‐freshwater boundary is a major biodiversity gradient and few groups have colonised both systems successfully. Fishes have transitioned between habitats repeatedly, diversifying in rivers, lakes and oceans over evolutionary time. However, their history of habitat colonisation and diversification is unclear based on available fossil and phylogenetic data. We estimate ancestral habitats and diversification and transition rates using a large‐scale phylogeny of extant fish taxa and one containing a massive number of extinct species. Extant‐only phylogenetic analyses indicate freshwater ancestry, but inclusion of fossils reveal strong evidence of marine ancestry in lineages now restricted to freshwaters. Diversification and colonisation dynamics vary asymmetrically between habitats, as marine lineages colonise and flourish in rivers more frequently than the reverse. Our study highlights the importance of including fossils in comparative analyses, showing that freshwaters have played a role as refuges for ancient fish lineages, a signal erased by extinction in extant‐only phylogenies.     

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.     

Species selection and random drift in macroevolution

Species selection resulting from trait‐dependent speciation and extinction is increasingly recognized as an important mechanism of phenotypic macroevolution. However, the recent bloom in statistical methods quantifying this process faces a scarcity of dynamical theory for their interpretation, notably regarding the relative contributions of deterministic versus stochastic evolutionary forces. I use simple diffusion approximations of birth‐death processes to investigate how the expected and random components of macroevolutionary change depend on phenotype‐dependent speciation and extinction rates, as can be estimated empirically. I show that the species selection coefficient for a binary trait, and selection differential for a quantitative trait, depend not only on differences in net diversification rates (speciation minus extinction), but also on differences in species turnover rates (speciation plus extinction), especially in small clades. The randomness in speciation and extinction events also produces a species‐level equivalent to random genetic drift, which is stronger for higher turnover rates. I then show how microevolutionary processes including mutation, organismic selection, and random genetic drift cause state transitions at the species level, allowing comparison of evolutionary forces across levels. A key parameter that would be needed to apply this theory is the distribution and rate of origination of new optimum phenotypes along a phylogeny.     

Early origin of viviparity and multiple reversions to oviparity in squamate reptiles

Viviparity has putatively evolved 115 times in squamates (lizards and snakes), out of only ~ 140 origins in vertebrates, and is apparently related to colder climates and other factors such as body size. Viviparity apparently evolves from oviparity via egg‐retention, and such taxa may thus still have the machinery to produce thick‐shelled eggs. Parity mode is also associated with variable diversification rates in some groups. We reconstruct ancestral parity modes accounting for state‐dependent diversification in a large‐scale phylogenetic analysis, and find strong support for an early origin of viviparity at the base of Squamata, and a complex pattern of subsequent transitions. Viviparous lineages have higher rates of speciation and extinction, and greater species turnover through time. Viviparity is associated with lower environmental and body temperatures in lizards and amphisbaenians, but not female mass. These results suggest that parity mode is a labile trait that shifts frequently in response to ecological conditions.     

Marine planktonic microbes survived climatic instabilities in the past

In the geological past, changes in climate and tectonic activity are thought to have spurred the tempo of evolutionary change among major taxonomic groups of plants and animals. However, the extent to which these historical contingencies increased the risk of extinction of microbial plankton species remains largely unknown. Here, I analyse fossil records of marine planktonic diatoms and calcareous nannoplankton over the past 65 million years from the world oceans and show that the probability of species' extinction is not correlated with secular changes in climatic instability. Further supporting these results, analyses of genera survivorship curves based on fossil data concurred with the predictions of a birth-death model that simulates the extinction of genera through time assuming stochastically constant rates of speciation and extinction. However, my results also show that these marine microbes responded to exceptional climatic contingencies in a manner that appears to have promoted net diversification. These results highlight the ability of marine planktonic microbes to survive climatic instabilities in the geological past, and point to different mechanisms underlying the processes of speciation and extinction in these micro-organisms.     

FiSSE: A simple nonparametric test for the effects of a binary character on lineage diversification rates

It is widely assumed that phenotypic traits can influence rates of speciation and extinction, and several statistical approaches have been used to test for correlations between character states and lineage diversification. Recent work suggests that model‐based tests of state‐dependent speciation and extinction are sensitive to model inadequacy and phylogenetic pseudoreplication. We describe a simple nonparametric statistical test (“FiSSE”) to assess the effects of a binary character on lineage diversification rates. The method involves computing a test statistic that compares the distributions of branch lengths for lineages with and without a character state of interest. The value of the test statistic is compared to a null distribution generated by simulating character histories on the observed phylogeny. Our tests show that FiSSE can reliably infer trait‐dependent speciation on phylogenies of several hundred tips. The method has low power to detect trait‐dependent extinction but can infer state‐dependent differences in speciation even when net diversification rates are constant. We assemble a range of macroevolutionary scenarios that are problematic for likelihood‐based methods, and we find that FiSSE does not show similarly elevated false positive rates. We suggest that nonparametric statistical approaches, such as FiSSE, provide an important complement to formal process‐based models for trait‐dependent diversification.     

Do saline taxa evolve faster? Comparing relative rates of molecular evolution between freshwater and marine eukaryotes

The major branches of life diversified in the marine realm, and numerous taxa have since transitioned between marine and freshwaters. Previous studies have demonstrated higher rates of molecular evolution in crustaceans inhabiting continental saline habitats as compared with freshwaters, but it is unclear whether this trend is pervasive or whether it applies to the marine environment. We employ the phylogenetic comparative method to investigate relative molecular evolutionary rates between 148 pairs of marine or continental saline versus freshwater lineages representing disparate eukaryote groups, including bony fish, elasmobranchs, cetaceans, crustaceans, mollusks, annelids, algae, and other eukaryotes, using available protein‐coding and noncoding genes. Overall, we observed no consistent pattern in nucleotide substitution rates linked to habitat across all genes and taxa. However, we observed some trends of higher evolutionary rates within protein‐coding genes in freshwater taxa—the comparisons mainly involving bony fish—compared with their marine relatives. The results suggest no systematic differences in substitution rate between marine and freshwater organisms.     

Innovation not recovery: dynamic redox promotes metazoan radiations

Environmental fluctuations in redox may reinforce rather than hinder evolutionary transitions, such that variability in near‐surface oceanic oxygenation can promote morphological evolution and novelty. Modern, low‐oxygen regions are heterogeneous and dynamic habitats that support low diversity and are inhabited by opportunistic and non‐skeletal metazoans. We note that several major radiation episodes follow protracted or repeating intervals (>1 million years) of persistent and dynamic shallow marine redox (oceanic anoxic events). These are also often associated with short‐lived mass‐extinction events (<0.5 million years) where skeletal benthic incumbents are removed, and surviving or newly evolved benthos initially inhabit transient oxic habitats. We argue that such intervals create critical opportunities for the generation of evolutionary novelty, followed by innovation and diversification. We develop a general model for redox controls on the distribution and structure of the shallow marine benthos in a dominantly anoxic world, and compile data from the terminal Ediacaran–mid‐Cambrian (∼560–509 Ma), late Cambrian–Ordovician (∼500–445 Ma), and Permo‐Triassic (∼255–205 Ma) to test these predictions. Assembly of phylogenetic data shows that prolonged and widespread anoxic intervals indeed promoted morphological novelty in soft‐bodied benthos, providing the ancestral stock for subsequently skeletonized lineages to appear as innovations once oxic conditions became widespread and stable, in turn promoting major evolutionary diversification. As a result, we propose that so‐called ‘recovery’ intervals after mass extinctions might be better considered as ‘innovation’ intervals.     

Larger brains spur species diversification in birds

Evidence is accumulating that species traits can spur their evolutionary diversification by influencing niche shifts, range expansions, and extinction risk. Previous work has shown that larger brains (relative to body size) facilitate niche shifts and range expansions by enhancing behavioral plasticity but whether larger brains also promote evolutionary diversification is currently backed by insufficient evidence. We addressed this gap by combining a brain size dataset for >1900 avian species worldwide with estimates of diversification rates based on two conceptually different phylogenetic‐based approaches. We found consistent evidence that lineages with larger brains (relative to body size) have diversified faster than lineages with relatively smaller brains. The best supported trait‐dependent model suggests that brain size primarily affects diversification rates by increasing speciation rather than decreasing extinction rates. In addition, we found that the effect of relatively brain size on species‐level diversification rate is additive to the effect of other intrinsic and extrinsic factors. Altogether, our results highlight the importance of brain size as an important factor in evolution and reinforce the view that intrinsic features of species have the potential to influence the pace of evolution.     

Species and shape diversification are inversely correlated among gobies and cardinalfishes (Teleostei: Gobiiformes)

Gobies and their relatives are significant components of nearshore marine, estuarine, and freshwater fish faunas in both tropical and temperate habitats worldwide. They are remarkable for their ability to adapt to and diversify in a wide range of environments. Among gobiiform clades, species diversities vary widely, ranging from two species in Kurtidae to more than 1,000 species in Gobiidae. There is also great variation in head and body shape and in environmental preferences (fresh, brackish, or marine habitats). In this study, I used a time-calibrated molecular phylogeny, coupled with morphometric and comparative analyses, to examine evolutionary rates of both speciation and morphological diversification among gobiiform lineages. Projection of the phylogeny onto a shape-derived morphospace shows that Gobioidei is morphometrically distinct from its sister taxon Apogonoidei, but that families within Gobioidei overlap in morphospace. Analysis of species diversification rates indicates that three rate shifts have occurred over the evolutionary history of Gobiiformes. Relative to the other lineages, Kurtidae has exhibited a slowdown in speciation, whereas both Apogonidae and Gobiidae?+?Gobionellidae have experienced an increase in diversification. Comparative analyses show that in Apogonidae and Gobiidae?+?Gobionellidae, increased speciation is correlated with diminished rates of morphological diversification, differently manifested in either clade and among the various sublineages. The elevation in speciation rates and diminishment in rates of morphological change in both Apogonidae and the clade Gobiidae?+?Gobionellidae are correlated with shifts to oceanic habitats from freshwater. This pattern is the complement to that seen across the global radiation of acanthomorph fishes in which a decrease in species diversification is associated with an increase in morphological disparity.     

Niche width impacts vertebrate diversification

Aim The size of the climatic niche of a species is a major factor determining its distribution and evolution. In particular, it has been proposed that niche width should be associated with the rate of species diversification. Here, we test whether species niche width affects the speciation and extinction rates of three main clades of vertebrates: amphibians, mammals and birds. Location Global. Methods We obtained the time‐calibrated phylogenies, IUCN conservation status, species distribution maps and climatic data for 2340 species of amphibians, 4563 species of mammals and 9823 species of birds. We computed the niche width for each species as the mean annual temperature across the species range. We estimated speciation, extinction and transition rates associated with lineages with either narrow (specialist) or wide (generalist) niches using phylogeny‐based birth–death models. We also tested if current conservation status was correlated with the niche width of species. Results We found higher net diversification rates in specialist species than in generalist species. This result was explained by both higher speciation rates (for the three taxonomic groups) and lower extinction rates (for mammals and birds only) in specialist than in generalist species. In contrast, current specialist species tended to be more threatened than generalist species. Main conclusions Our diversification analysis shows that the width of the climatic niche is strongly associated with diversification rates and may thus be a crucial factor for understanding the emergence of diversity patterns in vertebrates. The striking difference between our diversification results and current conservation status suggests that the current extinction process may be different from extinction rates estimated from the whole history of the group.     

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.     

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.     

DISENTANGLING THE EFFECTS OF KEY INNOVATIONS ON THE DIVERSIFICATION OF BROMELIOIDEAE (BROMELIACEAE)

The evolution of key innovations, novel traits that promote diversification, is often seen as major driver for the unequal distribution of species richness within the tree of life. In this study, we aim to determine the factors underlying the extraordinary radiation of the subfamily Bromelioideae, one of the most diverse clades among the neotropical plant family Bromeliaceae. Based on an extended molecular phylogenetic data set, we examine the effect of two putative key innovations, that is, the Crassulacean acid metabolism (CAM) and the water‐impounding tank, on speciation and extinction rates. To this aim, we develop a novel Bayesian implementation of the phylogenetic comparative method, binary state speciation and extinction, which enables hypotheses testing by Bayes factors and accommodates the uncertainty on model selection by Bayesian model averaging. Both CAM and tank habit were found to correlate with increased net diversification, thus fulfilling the criteria for key innovations. Our analyses further revealed that CAM photosynthesis is correlated with a twofold increase in speciation rate, whereas the evolution of the tank had primarily an effect on extinction rates that were found five times lower in tank‐forming lineages compared to tank‐less clades. These differences are discussed in the light of biogeography, ecology, and past climate change.     

Does migration promote or inhibit diversification? A case study involving the dominant radiation of temperate Southern Hemisphere freshwater fishes

Although theory predicts that dispersal has a pivotal influence on speciation and extinction rates, it can have contradictory effects on each, such that empirical quantification of its role is required. In many studies, dispersal reduction appears to promote diversification, although some comparisons of migratory and nonmigratory species suggest otherwise. We tested for a relationship between migratory status and diversification rate within the dominant radiation of temperate Southern Hemisphere freshwater fishes, the Galaxiidae. We reconstructed a molecular phylogeny comprising >95% of extant taxa, and applied State-dependent Speciation Extinction models to estimate speciation, extinction, and diversification rates. In contrast to some previous studies, we revealed higher diversification rates in nonmigratory lineages. The reduced gene flow experienced by nonmigratory galaxiids appears to have increased diversification under conditions of allopatry or local adaptation. Migratory galaxiid lineages, by contrast, are genetically homogeneous within landmasses, but may also be rarely able to diversify by colonizing other landmasses in the temperate Southern Hemisphere. Apparent contradictions among studies of dispersal-diversification relationships may be explained by the spatial context of study systems relative to species dispersal abilities, by means of the “intermediate dispersal” model; the accurate quantification of dispersal abilities will aid in the understanding of these proposed interactions.     

Primate diversification inferred from phylogenies and fossils

Biodiversity arises from the balance between speciation and extinction. Fossils record the origins and disappearance of organisms, and the branching patterns of molecular phylogenies allow estimation of speciation and extinction rates, but the patterns of diversification are frequently incongruent between these two data sources. I tested two hypotheses about the diversification of primates based on ～600 fossil species and 90% complete phylogenies of living species: (1) diversification rates increased through time; (2) a significant extinction event occurred in the Oligocene. Consistent with the first hypothesis, analyses of phylogenies supported increasing speciation rates and negligible extinction rates. In contrast, fossils showed that while speciation rates increased, speciation and extinction rates tended to be nearly equal, resulting in zero net diversification. Partially supporting the second hypothesis, the fossil data recorded a clear pattern of diversity decline in the Oligocene, although diversification rates were near zero. The phylogeny supported increased extinction ～34 Ma, but also elevated extinction ～10 Ma, coinciding with diversity declines in some fossil clades. The results demonstrated that estimates of speciation and extinction ignoring fossils are insufficient to infer diversification and information on extinct lineages should be incorporated into phylogenetic analyses.     

Apparent signal of competition limiting diversification after ecological transitions from marine to freshwater habitats

Adaptive radiations are typically triggered when a lineage encounters a significant range of open niche space (ecological opportunity), stemming from colonisation of new areas, extinction of competitors or key innovations. The most well-known of these is the colonisation of new areas, through either dispersal into new regions or the invasion of novel ecological regimes. One aspect of ecological opportunity that has rarely been studied, however, is the extent to which pre-existent competitors act to limit diversification in newly colonised adaptive zones. Herein, we show that in multiple geographically independent invasions of freshwaters by marine Sea Catfishes (Ariidae), rates of both morphological disparification and lineage diversification are inversely related to the presence and diversity of other freshwater fish lineages. Only in one region (Australia-New Guinea) with an otherwise depauperate freshwater fauna, has an ariid invasion gained any substantial traction. This is true at both regional and community scales, suggesting that competitive constraints may be an important factor regulating adaptive radiation.     

Linking the investigations of character evolution and species diversification

Variation in diversification rates is often studied by investigating traits related to species' ecology and life history. Often, however, it is unknown whether these traits evolve gradually or in punctuated bursts during speciation. Using phylogenetic data and species' present-day trait information, we present a novel approach to assessing the mode of character change while accounting for trait-dependent speciation and extinction. Our model, "Binary-State Speciation and Extinction-node enhanced state shift" (BiSSE-ness), estimates both the rate of change occurring along lineages and the probability of change occurring during speciation, as well as independent speciation and extinction rates for each character state. Using simulations, we found that BiSSE-ness is able to distinguish along-lineage and speciational change and accurately estimate the parameters associated with character change and diversification rates. We applied BiSSE-ness to an empirical primate data set and found evidence for along-lineage changes in primate mating systems and social behaviors, whereas shifts in habitat were associated with speciation. In cases where trait changes may be linked to the speciation process itself (e.g., niche-related traits), BiSSE-ness provides a suitable framework with which to simultaneously address questions regarding species diversification and character change.     

Loss of sexual recombination and segregation is associated with increased diversification in evening primroses

The loss of sexual recombination and segregation in asexual organisms has been portrayed as an irreversible process that commits asexually reproducing lineages to reduced diversification. We test this hypothesis by estimating rates of speciation, extinction, and transition between sexuality and functional asexuality in the evening primroses. Specifically, we estimate these rates using the recently developed BiSSE (Binary State Speciation and Extinction) phylogenetic comparative method, which employs maximum likelihood and Bayesian techniques. We infer that net diversification rates (speciation minus extinction) in functionally asexual evening primrose lineages are roughly eight times faster than diversification rates in sexual lineages, largely due to higher speciation rates in asexual lineages. We further reject the hypothesis that a loss of recombination and segregation is irreversible because the transition rate from functional asexuality to sexuality is significantly greater than zero and in fact exceeded the reverse rate. These results provide the first empirical evidence in support of the alternative theoretical prediction that asexual populations should instead diversify more rapidly than sexual populations because they are free from the homogenizing effects of sexual recombination and segregation. Although asexual reproduction may often constrain adaptive evolution, our results show that the loss of recombination and segregation need not be an evolutionary dead end in terms of diversification of lineages.