Peter C. Wainwright

Resolution of ray-finned fish phylogeny and timing of diversification

Ray-finned fishes make up half of all living vertebrate species. Nearly all ray-finned fishes are teleosts, which include most commercially important fish species, several model organisms for genomics and developmental biology, and the dominant component of marine and freshwater vertebrate faunas. Despite the economic and scientific importance of ray-finned fishes, the lack of a single comprehensive phylogeny with corresponding divergence-time estimates has limited our understanding of the evolution and diversification of this radiation. Our analyses, which use multiple nuclear gene sequences in conjunction with 36 fossil age constraints, result in a well-supported phylogeny of all major ray-finned fish lineages and molecular age estimates that are generally consistent with the fossil record. This phylogeny informs three long-standing problems: specifically identifying elopomorphs (eels and tarpons) as the sister lineage of all other teleosts, providing a unique hypothesis on the radiation of early euteleosts, and offering a promising strategy for resolution of the “bush at the top of the tree” that includes percomorphs and other spiny-finned teleosts. Contrasting our divergence time estimates with studies using a single nuclear gene or whole mitochondrial genomes, we find that the former underestimates ages of the oldest ray-finned fish divergences, but the latter dramatically overestimates ages for derived teleost lineages. Our time-calibrated phylogeny reveals that much of the diversification leading to extant groups of teleosts occurred between the late Mesozoic and early Cenozoic, identifying this period as the “Second Age of Fishes.”

TESTING FOR DIFFERENT RATES OF CONTINUOUS TRAIT EVOLUTION USING LIKELIHOOD

Abstract Rates of phenotypic evolution have changed throughout the history of life, producing variation in levels of morphological, functional, and ecological diversity among groups. Testing for the presence of these rate shifts is a key component of evaluating hypotheses about what causes them. In this paper, general predictions regarding changes in phenotypic diversity as a function of evolutionary history and rates are developed, and tests are derived to evaluate rate changes. Simulations show that these tests are more powerful than existing tests using standardized contrasts. The new approaches are distributed in an application called Brownie and in r8s.

Predicting patterns of prey use from morphology of fishes

Ecomorphological analyses that search for patterns of association between morphological and prey-use data sets will have a greater chance of understanding the causal relationships between form and diet if the morphological variables used have known consequences for feeding performance. We explore the utility of fish body size, mouth gape and jaw-lever mechanics in predicting patterns of prey use in two very different communities of fishes, Caribbean coral reef fishes, and species of the Centrarchidae that live in Lake Opinicon, Ontario. In spite of major differences in the spectrum of potential prey available, the centrarchids of Lake Opinicon show dietary transitions during ontogeny that are very similar to those seen among and within species of Caribbean groupers (Serranidae). The transition from small zooplankton to intermediate sized invertebrates and ultimately to fishes appears to be very general in ram-suction feeding fishes and is probably driven largely by the constraints of mouth size on prey capture ability. The jaw-lever systems for mouth opening and closing represent direct trade-offs for speed and force of jaw movement. The ratio of in-lever to out-lever in the opening system changes during ontogeny in bluegill, indicating that the mechanics and kinematics of jaw movement may change as well. Among 34 species of Caribbean reef fishes, biting species had jaw-closing ratios that favored force translation, while species that employ rapid-strike ram-suction had closing ratios that enhanced speed of closing and mouth opening ratios that favored a more rapid expansion of the mouth during the strike. We suggest that when prey are categorized into functional groups, reflecting the specific performance features that are important in capturing and handling them, and the differences among habitats in the available prey resource are taken into account, general patterns can be found in morphology-diet relations that cross phylogenetic boundaries.

CHAPTER 1 – The History and Biogeography of Fishes on Coral Reefs

[Extract] Coral reefs have been around since the Ordovician (Wood, 1999), and throughout their 450-million year history they have shared the oceans with fishes. Modern scleractinian-dominated coral reefs and their associated fish faunas represent only the latest manifestation of a reefal ecosystem. It is almost self-evident that history is important to coral reefs, as the reefs build on the skeletons of past generations. But what of the associated fauna? Today, fishes form an integral part of reef communities, modifying benthic community structure and forming a major conduit for the movement of energy and material. Like the reefs, reef fish faunas have been shaped by history, but this historical influence may not be as apparent. Although it is becoming increasingly clear that history plays an important role in structuring local communities (Rickleffs and Schluter, 1993a), its influence on the ecology and biogeography of fishes on coral reefs remains largely unknown. Most studies of reef systems have addressed the question of how biogeographic and ecological patterns are maintained; relatively few consider how these patterns arose or their consequences. However, it is the combination of these two factors, origins and maintenance, that offers the clearest understanding of the nature of biogeographic patterns in reef organisms. Studies of the history of coral reefs have been largely restricted to documenting the history of the reef builders, which have left an outstanding fossil record (Wood, 1999). The history of associated faunas, and fish in particular, is less clear. However, this is changing, primarily as a result of phylogenetic analyses of reef fishes and from a reappraisal of the fossil record.

Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes

Spiny-rayed fishes, or acanthomorphs, comprise nearly one-third of all living vertebrates. Despite their dominant role in aquatic ecosystems, the evolutionary history and tempo of acanthomorph diversification is poorly understood. We investigate the pattern of lineage diversification in acanthomorphs by using a well-resolved time-calibrated phylogeny inferred from a nuclear gene supermatrix that includes 520 acanthomorph species and 37 fossil age constraints. This phylogeny provides resolution for what has been classically referred to as the “bush at the top” of the teleost tree, and indicates acanthomorphs originated in the Early Cretaceous. Paleontological evidence suggests acanthomorphs exhibit a pulse of morphological diversification following the end Cretaceous mass extinction; however, the role of this event on the accumulation of living acanthomorph diversity remains unclear. Lineage diversification rates through time exhibit no shifts associated with the end Cretaceous mass extinction, but there is a global decrease in lineage diversification rates 50 Ma that occurs during a period when morphological disparity among fossil acanthomorphs increases sharply. Analysis of clade-specific shifts in diversification rates reveal that the hyperdiversity of living acanthomorphs is highlighted by several rapidly radiating lineages including tunas, gobies, blennies, snailfishes, and Afro-American cichlids. These lineages with high diversification rates are not associated with a single habitat type, such as coral reefs, indicating there is no single explanation for the success of acanthomorphs, as exceptional bouts of diversification have occurred across a wide array of marine and freshwater habitats.

MORPHOLOGY AND ECOLOGY: FUNCTIONAL BASIS OF FEEDING CONSTRAINTS IN CARIBBEAN LABRID FISHES'

This study examines the role of functional morphology of the feeding ap- paratus in constraining the food habits of Caribbean wrasses (Labridae) in the genus Hal- ichoeres. Like other wrasses, these fishes crush prey with powerful pharyngeal jaws. Esti- mates of pharyngeal jaw crushing strength were made, based on muscle size and architecture, for an ontogenetic series of fish from each of six species. The resultant scaling relationships indicated that, at any given body length, the six species differed in crushing strength. The ability to crush prey items was, therefore, predicted to vary among species. The relative importance of crushing strength and pharyngeal jaw gape in constraining predation was examined in laboratory feeding trials using three species that differed in estimated crushing strength: H. garnoti, H. bivittatus, and H. maculipinna. The feeding trials determined the largest individuals of three prey species that fishes could eat. Two hard-bodied prey species (a gastropod and a crab) and a softer bodied crab species were offered to wrasses. Feeding ability on the two hard-shelled prey was predicted best by crushing strength; fishes of equivalent crushing potential were able to eat the same maximum size prey, in spite of considerable interspecific variation in pharyngeal jaw gape and body length at any given crushing strength. The consequences of ontogenetic and interspecific differences in crushing ability for feeding habits were explored by analyzing the intestinal contents of fishes collected from the Belizean barrier reef. Crushing strength appeared to play a central role in constraining diets of these fishes. Ontogenetic diet analysis of three species revealed that fishes switched from soft-bodied to hard-shelled prey at 3-5 N crushing strength, even though this crushing strength occurred at a different body size and pharyngeal jaw gape in each species. This switch was followed by a reduction in dietary breadth as fishes specialized on hard- bodied prey. Few other Caribbean coral reef fishes are capable of crushing molluscs effec- tively. Wrasses thus utilize a relatively unexploited trophic niche on the prey-hardness resource dimension.

Many-to-One Mapping of Form to Function: A General Principle in Organismal Design? 1

Abstract We introduce the concept of many-to-one mapping of form to function and suggest that this emergent property of complex systems promotes the evolution of physiological diversity. Our work has focused on a 4-bar linkage found in labrid fish jaws that transmits muscular force and motion from the lower jaw to skeletal elements in the upper jaws. Many different 4-bar shapes produce the same amount of output rotation in the upper jaw per degree of lower jaw rotation, a mechanical property termed Maxillary KT. We illustrate three consequences of many-to-one mapping of 4-bar shape to Maxillary KT. First, many-to-one mapping can partially decouple morphological and mechanical diversity within clades. We found with simulations of 4-bars evolving on phylogenies of 500 taxa that morphological and mechanical diversity were only loosely correlated (R2 = 0.25). Second, redundant mapping permits the simultaneous optimization of more than one mechanical property of the 4-bar. Labrid fishes have capitalized on this flexibility, as illustrated by several species that have Maxillary KT = 0.8 but have different values of a second property, Nasal KT. Finally, many-to-one mapping may increase the influence of historical factors in determining the evolution of morphology. Using a genetic model of 4-bar evolution we exerted convergent selection on three different starting 4-bar shapes and found that mechanical convergence only created morphological convergence in simulations where the starting forms were similar. Many-to-one mapping is widespread in physiological systems and operates at levels ranging from the redundant mapping of genotypes to phenotypes, up to the morphological basis of whole-organism performance. This phenomenon may be involved in the uneven distribution of functional diversity seen among animal lineages.

HERBIVORE ABUNDANCE AND GRAZING INTENSITY ON A CARIBBEAN CORAL REEF

Herbivory is a primary factor in determining the structure of coral reef communities. Spatial variation among reef habitats in the intensity of herbivory has been documented, but underlying variation in species composition and abundance within the herbivore guild has received little attention. The distri- bution and relative abundances of herbivorous fishes and sea urchins across several habitats were studied on the Belizean barrier reef off the Caribbean coast of Central America. Marked variation in total herbivore density as well as major changes in the composition of the herbivore guild were found across reef habitats. Acanthurids (surgeonfishes) predominated in shallow areas (< 5 m) while scarids (parrotfishes) were dominant in deeper habitats. Significant differences among habitats in an experimental assay of grazing intensity were strongly correlated with herbivore abundance. The spatial distribution of herbivorous fishes across reef habitats does not appear to be simply explained by differences in reef topography, but may depend on complex interactions among proximity to nearby shelter, predator abundance, density of territorial competitors, and local availability of food resources.

Morphology predicts suction feeding performance in centrarchid fishes

SUMMARY Suction feeding fish differ in their capacity to generate subambient pressure while feeding, and these differences appear to relate to morphological variation. We developed a morphological model of force transmission in the fish head and parameterized it with measurements from individual fish. The model was applied to 45 individuals from five species of centrarchid fishes: Lepomis macrochirus, Lepomis punctatus, Lepomis microlophus, Micropterus salmoides and Pomoxis nigromaculatus. Measurements of epaxial cross-sectional area, epaxial moment arm, buccal area and buccal area moment arm were combined to estimate pressure generation capacity for individual fish. This estimation was correlated with pressure measured in fish feeding on elusive prey to test the models ability to predict pressure generation from morphology. The model explained differences in pressure generation found among individuals (P<0.001, r2=0.71) and produced a realistic estimate of normalized muscle stress during suction feeding (68.5±6.7 kPa). Fish with smaller mouths, larger epaxial cross-sectional area and longer epaxial moments, such as L. macrochirus (bluegill sunfish), generated lower pressures than fish with larger mouths, smaller cross-sectional area and shorter moments, such as M. salmoides (largemouth bass). These results reveal a direct trade-off between morphological requirements of feeding on larger prey (larger mouth size relative to body depth) and the ability to generate subambient pressure while suction feeding on elusive prey.

CHAPTER 2 – Ecomorphology of Feeding in Coral Reef Fishes

[Extract] O nce an observer gets past the stunning coloration, surely no feature inspires wonder in coral reef fishes so much as their morphological diversity. From large-mouthed groupers, to beaked parrotfish, barbeled goatfish, long-snouted trumpet fish, snaggle-toothed tusk fish, tube-mouthed planktivores, and fat-lipped sweet lips, coral reef fishes display a dazzling array of feeding structures. And, even the most casual fish watcher quickly gets a sense that this diversity means something, that fish form is related to what the animals eat. Clearly there is something to this impression, but just how are head and body morphology connected to prey choice? Are we really able to predict what a reef fish eats from studying its jaws and teeth? What are the major axes of diversification that are seen in reef fishes? Which morphological and ecological trophic types show the most common convergence? What ecological insights into reef processes have been gained from consideration of the functional design of fish feeding mechanisms? In this chapter we explore the relationship between fish anatomy and feeding habits. Our overall goal is to show how an understanding of the functional morphology of fish feeding mechanisms can be a powerful tool when considering several ecological issues in coral reef fish biology. We have attempted to identify generalities, the major patterns that seem to cut across phylogenetic and geographic boundaries. We begin by constructing a rationale for how functional morphology can be used to enhance our insight into some long-standing ecological questions. We then review the fundamental mechanical issues associated with feeding in fishes, and the basic design features of the head that are involved in prey capture and prey processing. This sets the stage for a discussion of how the mechanical properties of fish feeding systems have been modified during reef fish diversification. With this background, we consider some of the major conclusions that have been drawn from studies of reef fish feeding ecomorphology. Because of space constraints we discuss only briefly the role of sensory modalities--vision, olfaction, electroreception, and hearingmbut these are also significant and diverse elements of the feeding arsenal of coral reef fishes and entire review chapters could be written on each one.