Independent transitions to freshwater environments promote phenotypic divergence, not convergence, in stingrays.

Instances of convergent or parallel evolution provide a potent model system for exploring contingency and determinism in evolutionary biology. Likewise, the multiple, independent habitat transitions from saltwater to freshwater biomes offer opportunity for studying convergent evolution within and among different vertebrate lineages. For example, stingrays have invaded freshwater habitats multiple times across different continents, sometimes even several times within the same clade (e.g., Dasyatidae). We evaluated the frequency of saltwater-freshwater invasions in stingrays, compared ecological and phenotypic diversification among freshwater and saltwater lineages, and assessed the degree of convergence among freshwater species. Despite not being morphologically distinct from saltwater stingrays, freshwater stingrays do expand the margins of stingray morphological diversity. According to our data, trophic specialists occupied non-overlapping regions of morphospace, with piscivores and molluscivores being distinct from other diet guilds. Freshwater stingrays as a group did not strongly converge morphologically, neither did freshwater rays from different lineages which shared similar niches. These findings could be explained by there not being enough time for convergence to occur among more ancient and more recent freshwater lineages. Alternatively, the different ancestral bauplans of various freshwater ray lineages and weak selection on optimal phenotypes could promote contingency in the form of evolution along paths of least resistance.

Ecological and Phenotypic Diversification after a Continental Invasion in Neotropical Freshwater Stingrays.

Habitat transitions are key potential explanations for why some lineages have diversified and others have not-from Anolis lizards to Darwin's finches. The ecological ramifications of marine-to-freshwater transitions for fishes suggest evolutionary contingency: some lineages maintain their ancestral niches in novel habitats (niche conservatism), whereas others alter their ecological role. However, few studies have considered phenotypic, ecological, and lineage diversification concurrently to explore this issue. Here, we investigated the macroevolutionary history of the taxonomically and ecologically diverse Neotropical freshwater river rays (subfamily Potamotrygoninae), which invaded and diversified in the Amazon and other South American rivers during the late Oligocene to early Miocene. We generated a time-calibrated, multi-gene phylogeny for Potamotrygoninae and reconstructed evolutionary patterns of diet specialization. We measured functional morphological traits relevant for feeding and used comparative phylogenetic methods to examine how feeding morphology diversified over time. Potamotrygonine trophic and phenotypic diversity are evenly partitioned (non-overlapping) among internal clades for most of their history, until 20-16 mya, when more recent diversification suggests increasing overlap among phenotypes. Specialized piscivores (Heliotrygon and Paratrygon) evolved early in the history of freshwater stingrays, while later trophic specialization (molluscivory, insectivory, and crustacivory) evolved in the genus Potamotrygon. Potamotrygonins demonstrate ecological niche lability in diets and feeding apparatus; however, diversification has mostly been a gradual process through time. We suggest that competition is unlikely to have limited the potamotrygonine invasion and diversification in South America.

Proximate and ultimate causes of signal diversity in the electric fish Gymnotus.

A complete understanding of animal signal evolution necessitates analyses of both the proximate (e.g. anatomical and physiological) mechanisms of signal generation and reception, and the ultimate (i.e. evolutionary) mechanisms underlying adaptation and diversification. Here we summarize the results of a synthetic study of electric diversity in the species-rich neotropical electric fish genus Gymnotus. Our study integrates two research directions. The first examines the proximate causes of diversity in the electric organ discharge (EOD) - which is the carrier of both the communication and electrolocation signal of electric fishes - via descriptions of the intrinsic properties of electrocytes, electrocyte innervation, electric organ anatomy and the neural coordination of the discharge (among other parameters). The second seeks to understand the ultimate causes of signal diversity - via a continent-wide survey of species diversity, species-level phylogenetic reconstructions and field-recorded head-to-tail EOD (ht-EOD) waveforms (a common procedure for characterizing the communication component of electric fish EODs). At the proximate level, a comparative morpho-functional survey of electric organ anatomy and the electromotive force pattern of the EOD for 11 species (representing most major clades) revealed four distinct groups of species, each corresponding to a discrete area of the phylogeny of the genus and to a distinct type of ht-EOD waveform. At the ultimate level, our analyses (which emphasize the ht-EOD) allowed us to conclude that selective forces from the abiotic environment have had minimal impact on the communication component of the EOD. In contrast, selective forces of a biotic nature - imposed by electroreceptive predators, reproductive interference from heterospecific congeners, and sexual selection - may be important sources of diversifying selection on Gymnotus signals.

Molecular phylogenetics reveals a pattern of biome conservatism in New World anchovies (family Engraulidae).

Evolutionary transitions between marine and freshwater biomes are relatively rare events, yielding a widespread pattern of biome conservatism among aquatic organisms. We investigated biome transitions in anchovies (Engraulidae), a globally distributed clade of economically important fishes. Most anchovy species are near-shore marine fishes, but several exclusively freshwater species are known from tropical rivers of South America and were previously thought to be the product of six or more independent freshwater invasions. We generated a comprehensive molecular phylogeny for Engraulidae, including representatives from 15 of 17 currently recognized genera. Our data support previous hypotheses of higher-level relationships within Engraulidae, but show that most New World genera are not monophyletic and in need of revision. Ancestral character reconstruction reveals that New World freshwater anchovies are the product of a single marine to freshwater transition, supporting a pattern of biome conservatism. We argue that competition is the principal mechanism that regulates aquatic biome transitions on a continental scale.

The Casiquiare river acts as a corridor between the Amazonas and Orinoco river basins: biogeographic analysis of the genus Cichla.

The Casiquiare River is a unique biogeographic corridor between the Orinoco and Amazonas basins. We investigated the importance of this connection for Neotropical fishes using peacock cichlids (Cichla spp.) as a model system. We tested whether the Casiquiare provides a conduit for gene flow between contemporary populations, and investigated the origin of biogeographic distributions that span the Casiquiare. Using sequences from the mitochondrial control region of three focal species (C. temensis, C. monoculus, and C. orinocensis) whose distributions include the Amazonas, Orinoco, and Casiquiare, we constructed maximum likelihood phylograms of haplotypes and analyzed the populations under an isolation-with-migration coalescent model. Our analyses suggest that populations of all three species have experienced some degree of gene flow via the Casiquiare. We also generated a mitochondrial genealogy of all Cichla species using >2000 bp and performed a dispersal-vicariance analysis (DIVA) to reconstruct the historical biogeography of the genus. This analysis, when combined with the intraspecific results, supports two instances of dispersal from the Amazonas to the Orinoco. Thus, our results support the idea that the Casiquiare connection is important across temporal scales, facilitating both gene flow and the dispersal and range expansion of species.

Ancient trans-Atlantic flight explains locust biogeography: molecular phylogenetics of Schistocerca.

The desert locust (Schistocerca gregaria) has been an important agricultural pest at least since biblical times. Although the ecology, physiology and behaviour of this insect species have been well characterized, its biogeographical origins and evolutionary history are more obscure. Schistocerca gregaria occurs throughout Africa, the Middle East and Western Asia, but all other species in the genus Schistocerca are found in the New World. Because S. gregaria has the capacity for extreme long-distance movement associated with swarming behaviour, dispersal may have played an important role in determining current distribution patterns. Some authors have argued that S. gregaria is the product of an eastward trans-Atlantic dispersal from North America to Africa; others consider it more likely that the New World taxa are the product of westward dispersal from Africa. Here, we present a mitochondrial DNA phylogeny of Schistocerca species that supports the monophyly of New World species (including the Galapagos endemic Halmenus) relative to S. gregaria. In concert with observed patterns of molecular divergence, and in contrast to previous morphological studies, our analysis indicates a single trans-Atlantic flight from Africa to South America, followed by extensive speciation and ecological divergence in the New World.

Reinterpreting recapitulation: systematics of needlefishes and their allies (Teleostei: Beloniformes).

As needlefishes (Belonidae) grow, their jaws pass through a "halfbeak" stage that resembles the adult jaw condition of the closely related family of halfbeaks (Hemiramphidae). Based on this pattern, some authors have suggested that halfbeaks are "developmentally arrested" or paedomorphic needlefish derivatives, whereas others have supported the notion that needlefishes are descended from halfbeak-like ancestors and that needlefish ontogeny thereby recapitulates phylogeny. To test these ideas and to better understand evolutionary changes in jaw ontogeny, phylogenetic relationships among genera of needlefishes, sauries (Scomberesocidae), halfbeaks, and flyingfishes (Exocoetidae) were assessed using mitochondrial (cytochrome b and 16S), nuclear (Tmo-4C4), and morphological characters. The resultant tree provides several novel taxonomic findings: (1) flyingfishes appear to be nested within halfbeaks; (2) sauries appear to be nested within needlefishes; and (3) the Indo-West Pacific freshwater halfbeaks appear to be most closely related to the needlefish/saury clade. The structure of the tree falsifies the idea that halfbeaks are paedomorphic needlefishes. Instead, halfbeaks are basal relative to needlefishes, fitting the pattern predicted by the hypothesis of recapitulation. I discuss limitations to phylogenetic perspectives on recapitulation based on discrete character data by comparing aspects of von Baerian and Haeckelian views of the relation between ontogeny and phylogeny.

Molecular systematics, biogeography and population structure of neotropical freshwater needlefishes of the genus Potamorrhaphis.

Phylogenetic relationships of populations and species within Potamorrhaphis, a genus of freshwater South American needlefishes, were assessed using mitochondrial cytochrome b sequences. Samples were obtained from eight widely distributed localities in the Amazon and Orinoco rivers, and represented all three currently recognized species of Potamorrhaphis. The phylogeny of haplotypes corresponded imperfectly to current morphological species identities: haplotypes from P. guianensis, the most widespread species, did not make up a monophyletic clade. Geography played a strong role in structuring genetic variation: no haplotypes were shared between any localities, indicating restricted gene flow. Possible causes of this pattern include limited dispersal and the effects of current and past geographical barriers. The haplotype phylogeny also showed a complex relationship between fishes from different river basins. Based on the geographical distribution of clades, we hypothesize a connection between the middle Orinoco and Amazon via rivers of the Guianas. More ancient divergence events may have resulted from Miocene alterations of river drainage patterns. We also present limited data for two other Neotropical freshwater needlefish genera: Belonion and Pseudotylosurus. Pseudotylosurus showed evidence of substantial gene flow between distant localities, indicating ecological differences from Potamorrhaphis.