Suction feeding turned on its head: a functional novelty facilitates lower jaw protrusion.

Functional novelties play important roles in creating new ways for organisms to access resources. In fishes, jaw protrusion has been attributed to the massive diversity of suction-based feeding systems, facilitating the dominant mode of prey capture in this group. Nearly all fishes that feed by suction use upper jaw protrusion, achieved by rotation of the mandible at its base, which then transmits forward motion to independently mobile upper jaw bones. In this study, by contrast, we explore an unusual form of lower jaw protrusion in the freshwater invertivore, Nannocharax fasciatus, enabled by a novel intramandibular joint (IMJ). We combine morphological, kinematic, and biomechanical data to show that the added mobility created by the IMJ influences the pattern of suction-based prey capture movements and contributes to lower jaw protrusion (increasing it by 25%, based on biomechanical modeling). Interestingly, the upper jaw bones are fused in N. fasciatus and rotate about a single fixed joint, like the lower jaws of most other suction feeding fishes. We suggest that this vertical inversion of the jaw protrusion mechanism for ventrally directed suction-feeding on benthic prey is a likely exaptation, as the IMJ is used for biting in related taxa. This work highlights the ability of novelties to facilitate ecological specialization by enabling new functional capabilities.

Alternating regimes of shallow and deep-sea diversification explain a species-richness paradox in marine fishes.

The deep sea contains a surprising diversity of life, including iconic fish groups such as anglerfishes and lanternfishes. Still, >65% of marine teleost fish species are restricted to the photic zone <200 m, which comprises less than 10% of the ocean's total volume. From a macroevolutionary perspective, this paradox may be explained by three hypotheses: 1) shallow water lineages have had more time to diversify than deep-sea lineages, 2) shallow water lineages have faster rates of speciation than deep-sea lineages, or 3) shallow-to-deep sea transition rates limit deep-sea richness. Here we use phylogenetic comparative methods to test among these three non-mutually exclusive hypotheses. While we found support for all hypotheses, the disparity in species richness is better described as the uneven outcome of alternating phases that favored shallow or deep diversification over the past 200 million y. Shallow marine teleosts became incredibly diverse 100 million y ago during a period of warm temperatures and high sea level, suggesting the importance of reefs and epicontinental settings. Conversely, deep-sea colonization and speciation was favored during brief episodes when cooling temperatures increased the efficiency of the ocean's carbon pump. Finally, time-variable ecological filters limited shallow-to-deep colonization for much of teleost history, which helped maintain higher shallow richness. A pelagic lifestyle and large jaws were associated with early deep-sea colonists, while a demersal lifestyle and a tapered body plan were typical of later colonists. Therefore, we also suggest that some hallmark characteristics of deep-sea fishes evolved prior to colonizing the deep sea.

The rise of biting during the Cenozoic fueled reef fish body shape diversification.

Diversity of feeding mechanisms is a hallmark of reef fishes, but the history of this variation is not fully understood. Here, we explore the emergence and proliferation of a biting mode of feeding, which enables fishes to feed on attached benthic prey. We find that feeding modes other than suction, including biting, ram biting, and an intermediate group that uses both biting and suction, were nearly absent among the lineages of teleost fishes inhabiting reefs prior to the end-Cretaceous mass extinction, but benthic biting has rapidly increased in frequency since then, accounting for about 40% of reef species today. Further, we measured the impact of feeding mode on body shape diversification in reef fishes. We fit a model of multivariate character evolution to a dataset comprising three-dimensional body shape of 1,530 species of teleost reef fishes across 111 families. Dedicated biters have accumulated over half of the body shape variation that suction feeders have in just 18% of the evolutionary time by evolving body shape ∼1.7 times faster than suction feeders. As a possible response to the ecological and functional diversity of attached prey, biters have dynamically evolved both into shapes that resemble suction feeders as well as novel body forms characterized by lateral compression and small jaws. The ascendance of species that use biting mechanisms to feed on attached prey reshaped modern reef fish assemblages and has been a major contributor to their ecological and phenotypic diversification.

A novel intramandibular joint facilitates feeding versatility in the sixbar distichodus.

The intramandibular joint (IMJ) is a secondary point of movement between the two major bones of the lower jaw. It has independently evolved in several groups of teleost fishes, each time representing a departure from related species in which the mandible functions as a single structure rotating only at the quadratomandibular joint (QMJ). In this study, we examine kinematic consequences of the IMJ novelty in a freshwater characiform fish, the herbivorous Distichodus sexfasciatus. We combine traditional kinematic approaches with trajectory-based analysis of motion shapes to compare patterns of prey capture movements during substrate biting, the fish's native feeding mode, and suction of prey from the water column. We find that the IMJ enables complex jaw motions and contributes to feeding versatility by allowing the fish to modulate its kinematics in response to different prey and to various scenarios of jaw-substrate interaction. Implications of the IMJ include context-dependent movements of lower versus upper jaws, enhanced lower jaw protrusion, and the ability to maintain contact between the teeth and substrate throughout the jaw closing or biting phase of the motion. The IMJ in D. sexfasciatus appears to be an adaptation for removing attached benthic prey, consistent with its function in other groups that have evolved the joint. This study builds on our understanding of the role of the IMJ during prey capture and provides insights into broader implications of the innovative trait.

The deep sea is a hot spot of fish body shape evolution.

Deep-sea fishes have long captured our imagination with striking adaptations to life in the mysterious abyss, raising the possibility that this cold, dark ocean region may be a key hub for physiological and functional diversification. We explore this idea through an analysis of body shape evolution across ocean depth zones in over 3000 species of marine teleost fishes. We find that the deep ocean contains twice the body shape disparity of shallow waters, driven by elevated rates of evolution in traits associated with locomotion. Deep-sea fishes display more frequent adoption of forms suited to slow and periodic swimming, whereas shallow living species are concentrated around shapes conferring strong, sustained swimming capacity and manoeuvrability. Our results support long-standing impressions of the deep sea as an evolutionary hotspot for fish body shape evolution and highlight that factors like habitat complexity and ecological interactions are potential drivers of this adaptive diversification.

A Multifunction Trade-Off has Contrasting Effects on the Evolution of Form and Function.

Trade-offs caused by the use of an anatomical apparatus for more than one function are thought to be an important constraint on evolution. However, whether multifunctionality suppresses diversification of biomechanical systems is challenged by recent literature showing that traits more closely tied to trade-offs evolve more rapidly. We contrast the evolutionary dynamics of feeding mechanics and morphology between fishes that exclusively capture prey with suction and multifunctional species that augment this mechanism with biting behaviors to remove attached benthic prey. Diversification of feeding kinematic traits was, on average, over 13.5 times faster in suction feeders, consistent with constraint on biters due to mechanical trade-offs between biting and suction performance. Surprisingly, we found that the evolution of morphology contrasts directly with these differences in kinematic evolution, with significantly faster rates of evolution of head shape in biters. This system provides clear support for an often postulated, but rarely confirmed prediction that multifunctionality stifles functional diversification, while also illustrating the sometimes weak relationship between form and function. [Form-function evolution; geometric morphometrics; kinematic evolution; macroevolution; Ornstein-Uhlenbeck; RevBayes; suction feeding].

Decoupled jaws promote trophic diversity in cichlid fishes.

Functional decoupling of oral and pharyngeal jaws is widely considered to have expanded the ecological repertoire of cichlid fishes. But, the degree to which the evolution of these jaw systems is decoupled and whether decoupling has impacted trophic diversification remains unknown. Focusing on the large Neotropical radiation of cichlids, we ask whether oral and pharyngeal jaw evolution is correlated and how their evolutionary rates respond to feeding ecology. In support of decoupling, we find relaxed evolutionary integration between the two jaw systems, resulting in novel trait combinations that potentially facilitate feeding mode diversification. These outcomes are made possible by escaping the mechanical trade-off between force transmission and mobility, which characterizes a single jaw system that functions in isolation. In spite of the structural independence of the two jaw systems, results using a Bayesian, state-dependent, relaxed-clock model of multivariate Brownian motion indicate strongly aligned evolutionary responses to feeding ecology. So, although decoupling of prey capture and processing functions released constraints on jaw evolution and promoted trophic diversity in cichlids, the natural diversity of consumed prey has also induced a moderate degree of evolutionary integration between the jaw systems, reminiscent of the original mechanical trade-off between force and mobility.

The influence of size on body shape diversification across Indo-Pacific shore fishes.

Understanding the causes of body shape variability across the tree of life is one of the central issues surrounding the origins of biodiversity. One potential mechanism driving observed patterns of shape disparity is a strongly conserved relationship between size and shape. Conserved allometry has been shown to account for as much as 80% of shape variation in some vertebrate groups. Here, we quantify the amount of body shape disparity attributable to changes in body size across nearly 800 species of Indo-Pacific shore fishes using a phylogenetic framework to analyze 17 geometric landmarks positioned to capture general body shape and functionally significant features. In marked contrast to other vertebrate lineages, we find that changes in body size only explain 2.9% of the body shape variation across fishes, ranging from 3% to 50% within our 11 sampled families. We also find a slight but significant trend of decreasing rates of shape evolution with increasing size. Our results suggest that the influence of size on fish shape has largely been overwhelmed by lineage-specific patterns of diversification that have produced the modern landscape of highly diverse forms that we currently observe in nature.

DNA barcoding uncovers extensive cryptic diversity in the African long-fin tetra Bryconalestes longipinnis (Alestidae: Characiformes).

To investigate the presence of cryptic diversity in the African longfin-tetra Bryconalestes longipinnis, we employed DNA barcoding in a phylogeographic context, as well as geometric morphometrics, documenting for the first time genetic and body shape variation in the species. Analysis of cytochrome oxidase I gene (coI) sequence variation exposed extremely high levels of genetic differentiation among samples from across the geographic range of the species (up to 18%), certainly much greater than the traditionally employed c. 3% sequence divergence heuristic threshold for conspecifics. Phylogeographic analyses of coI data revealed eight clusters/clades that diverge by >4% and up to 18% (p-distance), potentially representing cryptic members of a species complex. A clear biogeographic pattern was also uncovered, in which the two main coI lineages corresponded geographically with the upper Guinea (UG) and lower Guinea (LG) ichthyofaunal provinces of continental Africa, respectively. Within each of these main lineages, however, no apparent phylogeographic structuring was found. Despite strong genetic differentiation, there is considerable overlap in body shape variation between UG and LG populations. For the most part, morphological variation does not match the strength of the molecular phylogeographic signal. Therefore, the ability to reliably utilise external body shape for regional delimitation remains elusive. Further anatomical investigation appears necessary to establish whether compelling diagnostic morphological features do exist between the divergent lineages of the B. longipinnis complex uncovered in this study.

Feeding ecology underlies the evolution of cichlid jaw mobility.

The fish feeding apparatus is among the most diverse functional systems in vertebrates. While morphological and mechanical variations of feeding systems are well studied, we know far less about the diversity of the motions that they produce. We explored patterns of feeding movements in African cichlids from Lakes Malawi and Tanganyika, asking whether the degree of kinesis is associated with dietary habits of species. We used geometric morphometrics to measure feeding kinesis as trajectories of shape change, based on 326 high-speed videos in 56 species. Cranial morphology was significantly related to feeding movements, both of which were distributed along a dietary axis associated with prey evasiveness. Small-mouthed cichlids that feed by scraping algae and detritus from rocks had low kinesis strikes, while large-mouthed species that eat large, evasive prey (fishes and shrimps) generated the greatest kinesis. Despite having higher overall kinesis, comparisons of trajectory shape (linearity) revealed that cichlids that eat mobile prey also displayed more kinematically conserved, or efficient, feeding motions. Our work indicates that prey evasiveness is strongly related to the evolution of cichlid jaw mobility, suggesting that this same relationship may explain the origins and diversity of highly kinetic jaws that characterize the super-radiation of spiny-rayed fishes.

Malagasy cichlids differentially limit impacts of body shape evolution on oral jaw functional morphology.

Patterns of trait covariation, such as integration and modularity, are vital factors that influence the evolution of vertebrate body plans. In functional systems, decoupling of morphological modules buffers functional change in one trait by reducing correlated variation with another. However, for complex morphologies with many-to-one mapping of form to function (MTOM), resistance to functional change may also be achieved by constraining morphological variation within a functionally stable region of morphospace. For this research, we used geometric morphometrics to evaluate the evolution of body shape and its relationship with jaw functional morphology in two independent radiations of endemic Malagasy cichlid (Teleostei: Cichlidae). Our results suggested that the two subfamilies used different strategies to mitigate impacts of body shape variation on a metric of jaw function, maxillary kinematic transmission (MKT): (1) modularity between cranial and postcranial morphologies, and (2) integration of body and jaw evolution, with jaw morphologies varying in a manner that limits change in MKT. This research shows that, unlike modularity, MTOM allows traits to retain strong evolutionary covariation while still reducing impacts on functionality. These results suggest that MTOM, and its influence on the evolution of correlated traits, is likely much more widespread than is currently understood.

Exploration of Trends in Interspecific Abundance-Occupancy Relationships Using Empirically Derived Simulated Communities.

The interspecific abundance-occupancy relationship (AOR) is a widely used tool that describes patterns of habitat utilization and, when evaluated over time, may be used to identify large-scale changes in community structure. Our primary goal for this research was to validate the utility of AORs as temporal indicators of community state. We used long-term survey data in four regions of the northwest Atlantic coastal shelf (NWACS) to estimate the diversity of spatial behaviors in each community, which we modeled with negative binomial (NB) distributions. NB parameters were used to generate time series data for simulated communities, from which AORs were then estimated and evaluated for temporal trends. We found that AORs from simulated communities were similar in year-to-year variation to empirical relationships. In order to further understand the role of spatial diversity in the generation of AOR trends, we did additional simulations where NB parameters were manually manipulated. In one instance, we ran simulations while holding species' parameters constant over time. This treatment effectively removed trends, suggesting that temporal change in community relationships was the result of genuine variation in intraspecific spatial use. In another set of simulations, we conducted a case study to evaluate the impact of a select group of schooling and spatially aggregating species on an especially rapid shift in AORs in the Gulf of Maine from 1973 to 1983. Removals of these species reduced the magnitudes of most trends, demonstrating their importance to observed community changes. This research directly links variation in AORs to distribution and density-related processes and provides a potentially powerful framework to identify community-level change and to test ecological and mechanistic hypotheses.

Re-evaluation of batoid pectoral morphology reveals novel patterns of diversity among major lineages.

Batoids (Chondrichthyes: Batoidea) are a diverse group of cartilaginous fishes which comprise a monophyletic sister lineage to all neoselachians or modern sharks. All species in this group possess anteroposteriorly expanded-pectoral fins, giving them a unique disc-like body form. Reliance on pectoral fins for propulsion ranges from minimal (sawfish) to almost complete dependence (skates and rays). A recent study on the diversity of planform pectoral fin shape in batoids compared overall patterns of morphological variation within the group. However, inconsistent pectoral homology prevented the study from accurately representing relationships within and among major batoid taxa. With previous work in mind, we undertook an independent investigation of pectoral form in batoids and evaluated the implications of shape diversity on locomotion and lifestyle, particularly in the skates (Rajoidei) and rays (Myliobatoidei). We used geometric morphometrics with sliding semilandmarks to analyze pectoral fin outlines and also calculate fin aspect ratios (AR), a functional trait linked to locomotion. In agreement with previous work, our results indicated that much of the evolution of batoid pectoral shape has occurred along a morphological axis that is closely related to AR. For species where kinematic data were available, both shape and AR were associated with swimming mode. This work further revealed novel patterns of shape variation among batoids, including strong bimodality of shape in rays, an intermediate location of skate species in the morphospace between benthic/demersal and pelagic rays, and approximately parallel shape trajectories in the benthic/demersal rays and skates. Finally, manipulation of landmarks verified the need for a consistent and accurate definition of homology for the outcome and efficacy of analyses of pectoral form and function in batoids.

Sexual dimorphism in sister species of Leucoraja skate and its relationship to reproductive strategy and life history.

Instances of sexual dimorphism occur in a great variety of forms and manifestations. Most skates (Batoidea: Rajoidei) display some level of body shape dimorphism in which the pectoral fins of mature males develop to create a distinct bell-shaped body not found in females. This particular form of dimorphism is present in each of the sister species Leucoraja erinacea and Leucoraja ocellata, but differences between sexes are much greater in the former. In order to understand the nature and potential causes of pectoral dimorphism, we used geometric morphometrics to investigate allometry of fin shape in L. erinacea and L. ocellata and its relationship to the development of reproductive organs, based on previous work on the bonnethead shark, Sphyrna tiburo. We found that allometric trajectories of overall pectoral shape were different in both species of skate, but only L. erinacea varied significantly with respect to endoskeleton development. Male maturation was characterized by a number of sex-specific morphological changes, which appeared concurrently in developmental timing with elongation of cartilage-supported claspers. We suggest that external sexual dimorphism of pectoral fins in skates is a byproduct of skeletal growth needed for clasper development. Further, the magnitude of male shape change appears to be linked to the differential life histories of species. This work reports for the first time that pectoral dimorphism is a persistent feature in rajoid fishes, occurring in varying degrees across several genera. Lastly, our results suggest that pectoral morphology may be useful as a relative indicator of reproductive strategy in some species.

A new species of Ptychochromis from southeastern Madagascar (Teleostei: Cichlidae).

We describe a new species in the endemic Malagasy cichlid genus Ptychochromis. Ptychochromis mainty, new species, is known from four individuals, all collected in the Fort Dauphin region of southeastern Madagascar, and shares a palatine morphology (eastern-type palatine) with other eastern congeners. Ptychochromis mainty is distinguished from all congeners by a nearly uniform dark brown to black pigmentation pattern in preservation and by the presence of a relatively continuous and expansive black longitudinal midlateral blotch in life, extending from the posterior margin of the opercle to the caudal peduncle. The new species is further distinguished from other eastern Ptychochromis species by having minimal or no overlap of the first supraneural with the dorsoposterior region of the supraoccipital crest (vs. marked overlap). We present a molecular-based phylogeny for all available Ptychochromis species, which supports the hypothesis that P. mainty is a distinct taxon. The new species is recovered as the sister taxon to P. grandidieri within a clade comprising species with an eastern-type palatine morphology. We present a geometric morphometric analysis that provides additional evidence to distinguish P. mainty from congeners.