ABSTRACT
The colonization of a novel geographic area is a classic source of ecological opportunity. Likewise, complex microhabitats are thought to promote biodiversity. We sought to reconcile these two predictions when they are naturally opposing outcomes. We assess the macroevolutionary consequences of an ancestral shift from benthic to pelagic microhabitat zones on rates of speciation and phenotypic evolution in North American minnows. Pelagic species have more similar phenotypes and slower rates of phenotypic evolution, but faster speciation rates, than benthic species. These are likely two independent, opposing responses to specialization along the benthic-pelagic axis, as rates of phenotypic evolution and speciation are not directly correlated. The pelagic zone is more structurally homogenous and offers less ecological opportunity, acting as an ecological dead end for minnows. In contrast, pelagic species may be more mobile and prone to dispersal and subsequent geographic isolation and, consequently, experience elevated instances of allopatric speciation. Microhabitat shifts can have decoupled effects on different dimensions of biodiversity, highlighting the need for nuance when interpreting the macroevolutionary consequences of ecological opportunity.
Subject(s)
Cyprinidae , Ecosystem , Genetic Speciation , Animals , Cyprinidae/genetics , Cyprinidae/physiology , Biological Evolution , Biodiversity , North America , PhenotypeABSTRACT
Almost nothing is known about the diets of bathypelagic fishes, but functional morphology can provide useful tools to infer ecology. Here we quantify variation in jaw and tooth morphologies across anglerfishes (Lophiiformes), a clade spanning shallow and deep-sea habitats. Deep-sea ceratioid anglerfishes are considered dietary generalists due to the necessity of opportunistic feeding in the food-limited bathypelagic zone. We found unexpected diversity in the trophic morphologies of ceratioid anglerfishes. Ceratioid jaws span a functional continuum ranging from species with numerous stout teeth, a relatively slow but forceful bite, and high jaw protrusibility at one end (characteristics shared with benthic anglerfishes) to species with long fang-like teeth, a fast but weak bite and low jaw protrusibility at the other end (including a unique 'wolftrap' phenotype). Our finding of high morphological diversity seems to be at odds with ecological generality, reminiscent of Liem's paradox (morphological specialization allowing organisms to have broader niches). Another possible explanation is that diverse ceratioid functional morphologies may yield similar trophic success (many-to-one mapping of morphology to diet), allowing diversity to arise through neutral evolutionary processes. Our results highlight that there are many ways to be a successful predator in the deep sea.
Subject(s)
Biological Evolution , Tooth , Animals , Phylogeny , Fishes , Ecosystem , Jaw/anatomy & histology , Feeding BehaviorABSTRACT
Hyphessobrycon is one of the most species rich and widely distributed genera in the family Characidae, with more than 160 species ranging from Veracruz, Mexico to Mar Chiquita Lagoon in Buenos Aires, Argentina. The majority of Hyphessobrycon diversity shows a cis-Andean distribution; only nine species are trans-Andean including H. compressus (Meek 1908). It is well established that Hyphessobrycon is not monophyletic but it has been suggested that natural groups can be identified within the larger Hyphessobrycon species group. In this study, we tested the monophyly of trans-Andean species of Hyphessobrycon and investigated the placement of H. compressus. We inferred the first phylogenomic hypothesis of trans-Andean Hyphessobrycon that includes nearly complete taxonomic sampling (eight of nine valid species) using ultraconserved elements (UCEs). We analyzed 75% (1682 UCEs), 90% (1258 UCEs), and 95% (838 UCEs) complete data matrices, and inferred phylogenomic hypotheses under concatenation and coalescent approaches. In all cases, we recovered the monophyly of trans-Andean Hyphessobrycon inclusive of H. compressus, strong support for three species groups, and evidence of cryptic diversity within the widespread H. compressus and H. condotensis. We used our phylogenomic hypothesis to investigate the biogeographic history of Hyphessobrycon in Middle America. Our ancestral range estimation analysis suggests a single event of cis- to trans-Andean colonization followed by stepwise colonization from the Pacific slope of northwestern South America (Chocó block) to northern Middle America (Maya block). Our work supports the recognition of the trans-Andean species as Hyphessobrycon sensu stricto and provides an evolutionary template to examine morphological characters that will allow us to better understand the diversity of Hyphessobrycon in Middle America.
Subject(s)
Characidae , Animals , Phylogeny , South America , Colombia , North AmericaABSTRACT
The macroevolutionary consequences of evolving in the deep-sea remain poorly understood and are compounded by the fact that convergent adaptations for living in this environment makes elucidating phylogenetic relationships difficult. Lophiiform anglerfishes exhibit extreme habitat and predatory specializations, including the use of a fin-spine system as a luring device and unique reproductive strategies where parasitic males attach and fuse to females. Despite their notoriety for these odd characteristics, evolutionary relationships among these fishes remain unclear. We sought to clarify the evolutionary history of Lophiiformes using data from 1000 ultraconserved elements and phylogenomic inference methods with particular interest paid to the Ceratioidei (deep-sea anglerfishes) and Antennarioidei (frogfishes and handfishes). At the suborder level, we recovered similar topologies in separate phylogenomic analyses: The Lophioidei (monkfishes) are the sister group to the rest of the Lophiiformes, Ogcocephaloidei (batfishes) and Antennarioidei (frogfishes) form a sister group, and Chaunacioidei (coffinfishes) and Ceratioidei (deep-sea anglerfishes) form a clade. The relationships we recover within the ceratioids disagree with most previous phylogenetic investigations, which used legacy phylogenetic markers or morphology. We recovered non-monophyletic relationships in the Antennarioidei and proposed three new families based on molecular and morphological evidence: Histiophrynidae, Rhycheridae, and Tathicarpidae. Antennariidae was re-evaluated to include what was known as Antennariinae, but not Histiophryninae. Non-bifurcating signal in splits network analysis indicated reticulations among and within suborders, supporting the complicated history of the Lophiiformes previously found with morphological data. Although we resolve relationships within Antennarioidei, Ceratioidei relationships remain somewhat unclear without better taxonomic sampling.
Subject(s)
Biological Evolution , Fishes , Animals , Ecosystem , Female , Humans , Male , Phylogeny , Predatory BehaviorABSTRACT
Balitorid loaches are a family of fishes that exhibit morphological adaptations to living in fast flowing water, including an enlarged sacral rib that creates a 'hip'-like skeletal connection between the pelvis and the axial skeleton. The presence of this sacral rib, the robustness of which varies across the family, is hypothesized to facilitate terrestrial locomotion seen in the family. Terrestrial locomotion in balitorids is unlike that of any known fish: the locomotion resembles that of terrestrial tetrapods. Emergence and convergence of terrestrial locomotion from water to land has been studied in fossils; however, studying balitorid walking provides a present-day natural laboratory to examine the convergent evolution of walking movements. We tested the hypothesis that balitorid species with more robust connections between the pelvic and axial skeleton (M3 morphotype) are more effective at walking than species with reduced connectivity (M1 morphotype). We predicted that robust connections would facilitate travel per step and increase mass support during movement. We collected high-speed video of walking in seven balitorid species to analyze kinematic variables. The connection between internal anatomy and locomotion on land are revealed herein with digitized video analysis, µCT scans, and in the context of the phylogenetic history of this family of fishes. Our species sampling covered the extremes of previously identified sacral rib morphotypes, M1 and M3. Although we hypothesized the robustness of the sacral rib to have a strong influence on walking performance, there was not a large reduction in walking ability in the species with the least modified rib (M1). Instead, walking kinematics varied between the two balitorid subfamilies with a generally more 'walk-like' behavior in the Balitorinae and more 'swim-like' behavior in the Homalopteroidinae. The type of terrestrial locomotion displayed in balitorids is unique among living fishes and aids in our understanding of the extent to which a sacral connection facilitates terrestrial walking.
Subject(s)
Cypriniformes , Animals , Biomechanical Phenomena , Locomotion , Phylogeny , Thailand , Walking , WaterABSTRACT
As an essential micronutrient for many organisms, sodium plays an important role in ecological and evolutionary dynamics. Although plants mediate trophic fluxes of sodium, from substrates to higher trophic levels, relatively little comparative research has been published about plant growth and sodium accumulation in response to variation in substrate sodium. Accordingly, we carried out a systematic review of plants' responses to variation in substrate sodium concentrations.We compared biomass and tissue-sodium accumulation among 107 cultivars or populations (67 species in 20 plant families), broadly expanding beyond the agricultural and model taxa for which several generalizations previously had been made. We hypothesized a priori response models for each population's growth and sodium accumulation as a function of increasing substrate NaCl and used Bayesian Information Criterion to choose the best model. Additionally, using a phylogenetic signal analysis, we tested for phylogenetic patterning of responses across taxa.The influence of substrate sodium on growth differed across taxa, with most populations experiencing detrimental effects at high concentrations. Irrespective of growth responses, tissue sodium concentrations for most taxa increased as sodium concentration in the substrate increased. We found no strong associations between the type of growth response and the type of sodium accumulation response across taxa. Although experiments often fail to test plants across a sufficiently broad range of substrate salinities, non-crop species tended toward higher sodium tolerance than domesticated species. Moreover, some phylogenetic conservatism was apparent, in that evolutionary history helped predict the distribution of total-plant growth responses across the phylogeny, but not sodium accumulation responses.Our study reveals that saltier plants in saltier soils proves to be a broadly general pattern for sodium across plant taxa. Regardless of growth responses, sodium accumulation mostly followed an increasing trend as substrate sodium levels increased.
ABSTRACT
The rheophilic hillstream loaches (Balitoridae) of South and Southeast Asia possess a range of pelvic girdle morphologies, which may be attributed to adaptations for locomotion against rapidly flowing water. Specifically, the connectivity of the pelvic plate (basipterygium) to the vertebral column via a sacral rib, and the relative size and shape of the sacral rib, fall within a spectrum of three discrete morphotypes: long, narrow rib that meets the basipterygium; thicker, slightly curved rib meeting the basipterygium; and robust crested rib interlocking with the basipterygium. Species in this third category with more robust sacral rib connections between the basipterygium and vertebral column are capable of walking out of water with a tetrapod-like lateral-sequence, diagonal-couplet gait. This behavior has not been observed in species lacking direct skeletal connection between the vertebrae and the pelvis. The phylogenetic positions of the morphotypes were visualized by matching the morphological features onto a novel hypothesis of relationships for the family Balitoridae. The morphotypes determined through skeletal morphology were correlated with patterns observed in the pelvic muscle morphology of these fishes. Transitions towards increasingly robust pelvic girdle attachment were coincident with a more anterior origin on the basipterygium and more lateral insertion of the muscles on the fin rays, along with a reduction of the superficial abductors and adductors with more posterior insertions. These modifications are expected to provide a mechanical advantage for generating force against the ground. Inclusion of the enigmatic cave-adapted balitorid Cryptotora thamicola into the most data-rich balitorid phylogeny reveals its closest relatives, providing insight into the origin of the skeletal connection between the axial skeleton and basipterygium.
Subject(s)
Bone and Bones/anatomy & histology , Cypriniformes/anatomy & histology , Muscles/anatomy & histology , Pelvis/anatomy & histology , Animals , Bone and Bones/diagnostic imaging , Cypriniformes/classification , Fourier Analysis , Muscles/diagnostic imaging , Pelvis/diagnostic imaging , Phylogeny , Principal Component Analysis , X-Ray MicrotomographyABSTRACT
Cave adaptation has evolved repeatedly across the Tree of Life, famously leading to pigmentation and eye degeneration and loss, yet its macroevolutionary implications remain poorly understood. We use the North American amblyopsid fishes, a family spanning a wide degree of cave adaptation, to examine the impact of cave specialization on the modes and tempo of evolution. We reconstruct evolutionary relationships using ultraconserved element loci, estimate the ancestral histories of eye-state, and examine the impact of cave adaptation on body shape evolution. Our phylogenomic analyses provide a well-supported hypothesis for amblyopsid evolutionary relationships. The obligate blind cavefishes form a clade and the cave-facultative eyed spring cavefishes are nested within the obligate cavefishes. Using ancestral state reconstruction, we find support for at least two independent subterranean colonization events within the Amblyopsidae. Eyed and blind fishes have different body shapes, but not different rates of body shape evolution. North American amblyopsids highlight the complex nature of cave-adaptive evolution and the necessity to include multiple lines of evidence to uncover the underlying processes involved in the loss of complex traits.