Abstract
From minute-to-minute changes, or across daily, seasonal, or geological timescales, animals are forced to navigate dynamic surroundings. Their abiotic environment is continually changing. ...These changes could include alterations to the substrates animals locomote on, flow dynamics of the microhabitats they feed in, or even altitudinal shifts over migration routes. The only constancy in any organism's day-to-day existence is the heterogeneity of the habitats they move through and the gradients in the physical media (e.g., air and water) they live in. We explored a broad range of organismal transitions across abiotic gradients and investigated how these organisms modify their form, function, and behavior to accommodate their surrounding media. We asked the following questions: (1) What are some challenges common to animals in changing media or moving between media? (2) What are common solutions to these recurring problems? (3) How often are these common solutions instances of either convergence or parallelism? Our symposium speakers explored these questions through critical analysis of numerous datasets spanning multiple taxa, timescales, and levels of analysis. After discussions with our speakers, we suggest that the role of physical principles (e.g., drag, gravity, buoyancy, and viscosity) in constraining morphology and shaping the realized niche has been underappreciated. We recommend that investigations of these transitions and corresponding adaptations should include comparisons at multiple levels of biological organization and timescale. Relatedly, studies of organisms that undergo habitat and substrate changes over ontogeny would be worthwhile to include in comparisons. Future researchers should ideally complement lab-based morphological and kinematic studies with observational and experimental approaches in the field. Synthesis of the findings of our speakers across multiple study systems, timescales, and transitional habitats suggests that behavioral modification and exaptation of morphology play key roles in modulating novel transitions between substrates.
Abstract
Hyperspectral data encode information from electromagnetic radiation (i.e., color) of any object in the form of a spectral signature; these data can then be used to distinguish among ...materials or even map whole landscapes. Although hyperspectral data have been mostly used to study landscape ecology, floral diversity and many other applications in the natural sciences, we propose that spectral signatures can be used for rapid assessment of faunal biodiversity, akin to DNA barcoding and metabarcoding. We demonstrate that spectral signatures of individual, live fish specimens can accurately capture species and clade-level differences in fish coloration, specifically among piranhas and pacus (Family Serrasalmidae), fishes with a long history of taxonomic confusion. We analyzed 47 serrasalmid species and could distinguish spectra among different species and clades, with the method sensitive enough to document changes in fish coloration over ontogeny. Herbivorous pacu spectra were more like one another than they were to piranhas; however, our method also documented interspecific variation in pacus that corresponds to cryptic lineages. While spectra do not serve as an alternative to the collection of curated specimens, hyperspectral data of fishes in the field should help clarify which specimens might be unique or undescribed, complementing existing molecular and morphological techniques.
Synopsis Constraints on phenotypic evolution can lead to patterns of convergent evolution, by limiting the “pool” of potential phenotypes in the face of endogenous (functional, developmental) or ...exogenous (competition, predation) selective pressures. Evaluation of convergence depends on integrating ecological and morphological data within a robust, comparative phylogenetic context. The staggering diversity of teleost fishes offers a multitude of lineages adapted for similar ecological roles and, therefore, offers numerous replicated evolutionary experiments for exploring phenotypic convergence. However, our understanding of fish feeding systems has been primarily shaped by marine species, with the monolithic exception of freshwater cichlids. Here we use piranhas and pacus (Serrasalmidae) to explore the evolution of different feeding ecologies and their morphological proxies in Neotropical freshwater environments. Specifically, we explore whether convergence is more widespread among plant-eating fishes, arising from strong constraints on phenotypic evolution in herbivores. Using osteological micro-computed tomographic imaging (μCT), we describe the major axes of morphological variation in pacus and piranhas, regarding their diet and feeding behaviors. Next, we evaluated whether herbivorous niches are less labile than other dietary guilds and whether herbivorous species’ phenotypes evolve at a slower evolutionary rate than other taxa. We then assess how convergent herbivorous taxa are, using three different suites of morphological characters (dental, jaw, and abdominal morphometrics). Ecologically, herbivory is not a dead end, exhibiting similar observed transition rates as those between carnivores and omnivores. However, we documented widespread convergence in herbivores and that herbivores have slower rates of phenotypic evolution than carnivores. Most instances of convergence are found in herbivorous taxa, specifically in frugivores and folivores. Moreover, instances of “complete” convergence, indicated by positive convergence metrics observed in more than one morphometric dataset, were only found in herbivores. Herbivores do appear to evolve under constrained circumstances, but this has not limited their ecological ability.
The Amazon and neighboring South American river basins harbor the world's most diverse assemblages of freshwater fishes. One of the most prominent South American fish families is the Serrasalmidae ...(pacus and piranhas), found in nearly every continental basin. Serrasalmids are keystone ecological taxa, being some of the top riverine predators as well as the primary seed dispersers in the flooded forest. Despite their widespread occurrence and notable ecologies, serrasalmid evolutionary history and systematics are controversial. For example, the sister taxon to serrasalmids is contentious, the relationships of major clades within the family are inconsistent across different methodologies, and half of the extant serrasalmid genera are suggested to be non-monophyletic. We analyzed exon capture to reexamine the evolutionary relationships among 63 (of 99) species across all 16 serrasalmid genera and their nearest outgroups, including multiple individuals per species to account for cryptic lineages. To reconstruct the timeline of serrasalmid diversification, we time-calibrated this phylogeny using two different fossil-calibration schemes to account for uncertainty in taxonomy with respect to fossil teeth. Finally, we analyzed diet evolution across the family and comment on associated changes in dentition, highlighting the ecomorphological diversity within serrasalmids. We document widespread non-monophyly of genera within Myleinae, as well as between Serrasalmus and Pristobrycon, and propose that reliance on traits like teeth to distinguish among genera is confounded by ecological homoplasy, especially among herbivorous and omnivorous taxa. We clarify the relationships among all serrasalmid genera, propose new subfamily affiliations, and support hemiodontids as the sister taxon to Serrasalmidae. Characiformes; exon capture; ichthyochory; molecular time-calibration; piscivory..
Brain anatomy provides key evidence for the relationships between ray-finned fishes
, but two major limitations obscure our understanding of neuroanatomical evolution in this major vertebrate group. ...First, the deepest branching living lineages are separated from the group's common ancestor by hundreds of millions of years, with indications that aspects of their brain morphology-like other aspects of their anatomy
-are specialized relative to primitive conditions. Second, there are no direct constraints on brain morphology in the earliest ray-finned fishes beyond the coarse picture provided by cranial endocasts: natural or virtual infillings of void spaces within the skull
. Here we report brain and cranial nerve soft-tissue preservation in Coccocephalus wildi, an approximately 319-million-year-old ray-finned fish. This example of a well-preserved vertebrate brain provides a window into neural anatomy deep within ray-finned fish phylogeny. Coccocephalus indicates a more complicated pattern of brain evolution than suggested by living species alone, highlighting cladistian apomorphies
and providing temporal constraints on the origin of traits uniting all extant ray-finned fishes
. Our findings, along with a growing set of studies in other animal groups
, point to the importance of ancient soft tissue preservation in understanding the deep evolutionary assembly of major anatomical systems outside of the narrow subset of skeletal tissues
.
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.
Abstract
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.
Gut morphology frequently reflects the food organisms digest. Gizzards are organs of the gut found in archosaurs and fishes that mechanically reduce food to aid digestion. Gizzards are thought to ...compensate for edentulism and/or provide an advantage when consuming small, tough food items (e.g., phytoplankton and algae). It is unknown how widespread gizzards are in fishes and how similar these structures are among different lineages. Here, we investigate the distribution of gizzards across bony fishes to (1) survey different fishes for gizzard presence, (2) compare the histological structure of gizzards in three species, (3) estimate how often gizzards have evolved in fishes, and (4) explore whether anatomical and ecological traits like edentulism and microphagy predict gizzard presence. According to our analyses, gizzards are rare across bony fishes, evolving only six times in a broad taxonomic sampling of 51 species, and gizzard presence is not clearly correlated with factors like gut length or dentition. We find that gizzard morphology varies among the lineages where one is present, both macroscopically (presence of a crop) and microscopically (varying tissue types). We conclude that gizzards likely aid in the mechanical reduction of food in fishes that have lost an oral dentition in their evolutionary past; however, the relative scarcity of gizzards suggests they are just one of many possible solutions for processing tough, nutrient-poor food items. Gizzards have long been present in the evolutionary history of fishes, can be found in a wide variety of marine and freshwater clades, and likely have been overlooked in many taxa.
Biological armours are potent model systems for understanding the complex series of competing demands on protective exoskeletons; after all, armoured organisms are the product of millions of years of ...refined engineering under the harshest conditions. Fishes are no strangers to armour, with various types of armour plating common to the 400-500 Myr of evolution in both jawed and jawless fishes. Here, we focus on the poachers (Agonidae), a family of armoured fishes native to temperate waters of the Pacific rim. We examined armour morphology, body stiffness and swimming performance in the northern spearnose poacher (
) over ontogeny. As juveniles, these fishes make frequent nocturnal forays into the water column in search of food, while heavily armoured adults are bound to the benthos. Most armour dimensions and density increase with body length, as does body stiffness. Juvenile poachers have enlarged spines on their armour whereas adults invest more mineral in armour plate bases. Adults are stiffer and accelerate faster than juveniles with an anguilliform swimming mode. Subadults more closely approximate adults more than smaller juveniles, with regards to both swimming and armour mechanics. Poacher armour serves multiple functions over ontogeny, from facilitating locomotion, slowing sinking and providing defence.
All stingrays in the family Myliobatidae are durophagous, consuming bivalves and gastropods, as well as decapod crustaceans. Durophagous rays have rigid jaws, flat teeth that interlock to form ...pavement-like tooth plates, and large muscles that generate bite forces capable of fracturing stiff biological composites (e.g. mollusk shell). The relative proportion of different prey types in the diet of durophagous rays varies between genera, with some stingray species specializing on particular mollusk taxa, while others are generalists. The tooth plate module provides a curved occlusal surface on which prey is crushed, and this curvature differs significantly among myliobatids. We measured the effect of jaw curvature on prey-crushing success in durophagous stingrays. We milled aluminum replica jaws rendered from computed tomography scans, and crushed live mollusks, three-dimensionally printed gastropod shells, and ceramic tubes with these fabricated jaws. Our analysis of prey items indicate that gastropods were consistently more difficult to crush than bivalves (i.e. were stiffer), but that mussels require the greatest work-to-fracture. We found that replica shells can provide an important proxy for investigations of failure mechanics. We also found little difference in crushing performance between jaw shapes, suggesting that disparate jaws are equally suited for processing different types of shelled prey. Thus, durophagous stingrays exhibit a many-to-one mapping of jaw morphology to mollusk crushing performance.