Comparative dynamics of suction feeding in marine and freshwater three-spined stickleback, Gasterosteus aculeatus: kinematics and geometric morphometrics

Abstract

Locomotion and feeding are key axes of diversity among fishes, and these are commonly integrated for successful prey capture. However, little is known about biomechanical variation among highly ecologically divergent populations of fishes. Three-spined stickleback, Gasterosteus aculeatus, is an ideal species for teasing apart the relationships between ecology, form and function, given the numerous independent invasions of freshwater lakes and streams from a marine ancestor. These natural replicates afford the opportunity to isolate convergence and/or many-to-one mapping of form to function. To explore the divergence between marine and freshwater stickleback, we investigated the differences in suction feeding kinematics and ram speed among individuals from replicates of both habitats. Feeding sequences were obtained using a high-speed camera, and microcomputed tomography was used to assess three-dimensional geometric morphometrics. Prey capture kinematics of marine and freshwater stickleback differed significantly, with marine individuals consistently exhibiting faster ram speeds, larger gapes, more jaw protrusion, and greater magnitudes and speeds of cranial rotation. These are consistent with an attack strategy aimed at evasive prey. In addition, populations exhibited significant morphological divergence, but not always along the marinefreshwater axis of divergence. Thus, there appears to be a mismatch between morphology and function. Together, our approach has revealed the dynamic kinematic divergence of marine and freshwater stickleback and how functional studies can be used to predict ecology.

Feeding ecology underlies the evolution of cichlid jaw mobility

“…These include, ecologically associated convergence and divergence in feeding kinematics (Norton and Brainerd ; Higham et al. ), strong links between modes of feeding kinesis and mouth size and morphology (Norton ), and the staging of distinct feeding movements (e.g., Lauder and Liem ; Cook ; Wilga and Motta ; Flammang et al. ).…”

“…In many respects, this work demonstrates recurring themes of fish feeding mechanics that have been observed over decades of kinematic and functional research. These include, ecologically associated convergence and divergence in feeding kinematics (Norton and Brainerd 1993;Higham et al 2017), strong links between modes of feeding kinesis and mouth size and morphology (Norton 1991), and the staging of distinct feeding movements (e.g., Lauder and Liem 1981;Cook 1996;Wilga and Motta 2000;Flammang et al 2009). Given that the approach used in the current study integrates various morphological features that comprise the feeding apparatus, we expected (and found) important distinctions from previous research on the same system that focused on a single component, upper jaw kinesis .…”

“…; Wilga and Motta ; Higham et al. ). While appropriate for assessing relative contributions of different components of the feeding apparatus, this approach is limited in its ability to treat this complex structure as the integrated system that it is.…”

“…However, the treatment of morphological data itself has not experienced equivalent levels of innovation. Standard procedure in many kinematic studies is to measure temporal changes for multiple disparate morphological features during an activity (e.g., Liem 1979;Lauder 1980;Wainwright et al 1991;Wilga and Motta 2000;Higham et al 2017). While appropriate for assessing relative contributions of different components of the feeding apparatus, this approach is limited in its ability to treat this complex structure as the integrated system that it is.…”

Rapid Divergence of Predator Functional Traits Affects Prey Composition in Aquatic Communities

“…The threespine stickleback (Gasterosteus aculeatus) is a particularly useful starting point for integrative analyses of the community consequences of consumer trait evolution. Previous work with stickleback has studied trait utility for a limited set of traits, including body size (Schluter 1993), gill raker characteristics (Robinson 2000), and jaw kinematics Higham et al 2017) as well as the heritability (Schluter et al 2004;Berner et al 2010Berner et al , 2011 and plasticity (Day et al 1994;Wund et al 2012;Laskowski and Bell 2013;Lucek et al 2014b) of these traits in a variety of environmental contexts. A separate body of work has also investigated the ecosystem effects of closely related stickleback species (Harmon et al 2009;Des Roches et al 2013), lineages (Best et al 2017), and ecotypes (Matthews et al 2016;Brunner et al 2017).…”