An official website of the United States government
ABSTRACT Understanding how organismal traits determine performance and, ultimately, fitness is a fundamental goal of evolutionary eco-morphology. However, multiple traits can interact in non-linear and context-dependent ways to affect performance, hindering efforts to place natural populations with respect to performance peaks or valleys. Here, we used an established mechanistic model of suction-feeding performance (SIFF) derived from hydrodynamic principles to estimate a theoretical performance landscape for zooplankton prey capture. This performance space can be used to predict prey capture performance for any combination of six morphological and kinematic trait values. We then mapped in situ high-speed video observations of suction feeding in a natural population of a coral reef zooplanktivore, Chromis viridis, onto the performance space to estimate the population's location with respect to the topography of the performance landscape. Although the kinematics of the natural population closely matched regions of high performance in the landscape, the population was not located on a performance peak. Individuals were furthest from performance peaks on the peak gape, ram speed and mouth opening speed trait axes. Moreover, we found that the trait combinations in the observed population were associated with higher performance than expected by chance, suggesting that these combinations are under selection. Our results provide a framework for assessing whether natural populations occupy performance optima.
more »
« less
Beyond Suction-Feeding Fishes: Identifying New Approaches to Performance Integration During Prey Capture in Aquatic Vertebrates
Abstract Organisms are composed of hierarchically arranged component parts that must work together to successfully achieve whole organism functions. In addition to integration among individual parts, some ecological demands require functional systems to work together in a type of inter-system performance integration. While performance can be measured by the ability to successfully accomplish ecologically relevant tasks, integration across performance traits can provide a deeper understanding of how these traits allow an organism to survive. The ability to move and the ability to consume food are essential to life, but during prey capture these two functions are typically integrated. Suction-feeding fishes have been used as a model of these interactions, but it is unclear how other ecologically relevant scenarios might reduce or change integration. To stimulate further research into these ideas, we highlight three contexts with the potential to result in changes in integration and underlying performance traits: (1) behavioral flexibility in aquatic feeding modes for capturing alternative prey types, (2) changes in the physical demands imposed by prey capture across environments, and (3) secondary adaptation for suction prey capture behaviors. These examples provide a broad scope of potential drivers of integration that are relevant to selection pressures experienced across vertebrate evolution. To demonstrate how these ideas can be applied and stimulate hypotheses, we provide observations from preliminary analyses of locally adapted populations of Trinidadian guppies (Poecilia reticulata) capturing prey using suction and biting feeding strategies and an Atlantic mudskipper (Periophthalmus barbarus) capturing prey above and below water. We also include a re-analysis of published data from two species of secondarily aquatic cetaceans, beluga whales (Delphinapterus leucas) and Pacific white-sided dolphins (Lagenorhynchus obliquidens), to examine the potential for secondary adaptation to affect integration in suction prey capture behaviors. Each of these examples support the broad importance of integration between locomotor and feeding performance but outline new ways that these relationships can be important when suction demands are reduced or altered. Future work in these areas will yield promising insights into vertebrate evolution and we hope to encourage further discussion on possible avenues of research on functional integration during prey capture.
more »
« less
- Award ID(s):
- 1832822
- PAR ID:
- 10115356
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 2
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- p. 456-472
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Suction feeding in ray-finned fishes requires substantial muscle power for fast and forceful prey capture. The axial musculature located immediately behind the head has been long known to contribute some power for suction feeding, but recent XROMM and fluoromicrometry studies found nearly all the axial musculature (over 80%) provides effectively all (90–99%) of the power for high-performance suction feeding. The dominance of axial power suggests a new framework for studying the musculoskeletal biomechanics of fishes: the form and function of axial muscles and bones should be analysed for power production in feeding (or at least as a compromise between swimming and feeding), and cranial muscles and bones should be analysed for their role in transmitting axial power and coordinating buccal expansion. This new framework is already yielding novel insights, as demonstrated in four species for which suction power has now been measured. Interspecific comparisons suggest high suction power can be achieved in different ways: increasing the magnitude of suction pressure or the rate of buccal volume change, or both (as observed in the most powerful of these species). Our framework suggests that mechanical and evolutionary interactions between the head and the body, and between the swimming and feeding roles of axial structures, may be fruitful areas for continued study.more » « less
-
Abstract Suction feeding and gill ventilation in teleosts are functionally coupled, meaning that there is an overlap in the structures involved with both functions. Functional coupling is one type of morphological integration, a term that broadly refers to any covariation, correlation, or coordination among structures. Suction feeding and gill ventilation exhibit other types of morphological integration, including functional coordination (a tendency of structures to work together to perform a function) and evolutionary integration (a tendency of structures to covary in size or shape across evolutionary history). Functional coupling, functional coordination, and evolutionary integration have each been proposed to limit morphological diversification to some extent. Yet teleosts show extraordinary cranial diversity, suggesting that there are mechanisms within some teleost clades that promote morphological diversification, even within the highly integrated suction feeding and gill ventilatory systems. To investigate this, we quantified evolutionary integration among four mechanical units associated with suction feeding and gill ventilation in a diverse clade of benthic, primarily suction-feeding fishes (Cottoidei; sculpins and relatives). We reconstructed cottoid phylogeny using molecular data from 108 species, and obtained 24 linear measurements of four mechanical units (jaws, hyoid, opercular bones, and branchiostegal rays) from micro-CT reconstructions of 44 cottoids and 1 outgroup taxon. We tested for evolutionary correlation and covariation among the four mechanical units using phylogenetically corrected principal component analysis to reduce the dimensionality of measurements for each unit, followed by correlating phylogenetically independent contrasts and computing phylogenetic generalized least squares models from the first principle component axis of each of the four mechanical units. The jaws, opercular bones, and branchiostegal rays show evolutionary integration, but the hyoid is not positively integrated with these units. To examine these results in an ecomorphological context, we used published ecological data in phylogenetic ANOVA models to demonstrate that the jaw is larger in fishes that eat elusive or grasping prey (e.g., prey that can easily escape or cling to the substrate) and that the hyoid is smaller in intertidal and hypoxia-tolerant sculpins. Within Cottoidei, the relatively independent evolution of the hyoid likely has reduced limitations on morphological evolution within the highly morphologically integrated suction feeding and gill ventilatory systems.more » « less
-
Since Darwin, biologists have sought to understand the evolution and origins of phenotypic adaptations. The skull is particularly diverse due to intense natural selection on feeding biomechanics. We investigated the genetic and molecular origins of trophic adaptation using Lake Malawi cichlids, which have undergone an exemplary evolutionary radiation. We analyzed morphological differences in the lateral and ventral head shape among an insectivore that eats by suction feeding, an obligate biting herbivore, and their F2 hybrids. We identified variation in a series of morphological traits—including mandible width, mandible length, and buccal length—that directly affect feeding kinematics and function. Using quantitative trait loci (QTL) mapping, we found that many genes of small effects influence these craniofacial adaptations. Intervals for some traits were enriched in genes related to potassium transport and sensory systems, the latter suggesting co-evolution of feeding structures and sensory adaptations for foraging. Despite these indications of co-evolution of structures, morphological traits did not show covariation. Furthermore, phenotypes largely mapped to distinct genetic intervals, suggesting that a common genetic basis does not generate coordinated changes in shape. Together, these suggest that craniofacial traits are mostly inherited as separate modules, which confers a high potential for the evolution of morphological diversity. Though these traits are not restricted by genetic pleiotropy, functional demands of feeding and sensory structures likely introduce constraints on variation. In all, we provide insights into the quantitative genetic basis of trophic adaptation, identify mechanisms that influence the direction of morphological evolution, and provide molecular inroads to craniofacial variation.more » « less
-
null (Ed.)Abstract Suction feeding has evolved independently in two highly disparate animal and plant systems, aquatic vertebrates and carnivorous bladderworts. We review the suction performance of animal and plant suction feeders to explore biomechanical performance limits for aquatic feeders based on morphology and kinematics, in the context of current knowledge of suction feeding. While vertebrates have the greatest diversity and size range of suction feeders, bladderworts are the smallest and fastest known suction feeders. Body size has profound effects on aquatic organismal function, including suction feeding, particularly in the intermediate flow regime that tiny organisms can experience. A minority of tiny organisms suction feed, consistent with model predictions that generating effective suction flow is less energetically efficient and also requires more flow-rate specific power at small size. Although the speed of suction flows generally increases with body and gape size, some specialized tiny plant and animal predators generate suction flows greater than those of suction feeders 100 times larger. Bladderworts generate rapid flow via high-energy and high-power elastic recoil and suction feed for nutrients (relying on photosynthesis for energy). Small animals may be limited by available muscle energy and power, although mouth protrusion can offset the performance cost of not generating high suction pressure. We hypothesize that both the high energetic costs and high power requirements of generating rapid suction flow shape the biomechanics of small suction feeders, and that plants and animals have arrived at different solutions due in part to their different energy budgets.more » « less
