Convergent evolution in mechanical design of lamnid sharks and tunas

Donley, Jeanine M.; Sepúlveda, Chugey A.; Konstantinidis, Peter; Gemballa, Sven; Shadwick, Robert E.

doi:10.1038/nature02435

Cited by 141 publications

(138 citation statements)

References 19 publications

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“…2) and thunniform swimming mode (where lateral movements are largely confined to the caudal region) associated with a unique force-transmission system from RM to the caudal region (25).…”

Section: Resultsmentioning

confidence: 99%

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Watanabe

Goldman

Caselle

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

109

139

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Despite long evolutionary separations, several sharks and tunas share the ability to maintain slow-twitch, aerobic red muscle (RM) warmer than ambient water. Proximate causes of RM endothermy are well understood, but ultimate causes are unclear. Two advantages often proposed are thermal niche expansion and elevated cruising speeds. The thermal niche hypothesis is generally supported, because fishes with RM endothermy often exhibit greater tolerance to broad temperature ranges. In contrast, whether fishes with RM endothermy cruise faster, and achieve any ecological benefits from doing so, remains unclear. Here, we compiled data recorded by modern animal-tracking tools for a variety of free-swimming marine vertebrates. Using phylogenetically informed allometry, we show that both cruising speeds and maximum annual migration ranges of fishes with RM endothermy are 2-3 times greater than fishes without it, and comparable to nonfish endotherms (i.e., penguins and marine mammals). The estimated cost of transport of fishes with RM endothermy is twice that of fishes without it. We suggest that the high energetic cost of RM endothermy in fishes is offset by the benefit of elevated cruising speeds, which not only increase prey encounter rates, but also enable larger-scale annual migrations and potentially greater access to seasonally available resources. marine predator | swim speed | migration | body temperature I n 1835, the British physician John Davy reported that skipjack tuna have body temperatures 10°C higher than ambient waters and considered this fish an exception to the general rule that fishes are cold-blooded (1). It is currently known that at least 14 species of tuna (family Scombridae) and five species of shark (four species in the family Lamnidae and one species in the family Alopiidae) have the ability to retain metabolic heat via vascular countercurrent heat exchangers, and to maintain the temperature of slow-twitch, aerobic red muscle (hereafter denoted RM) significantly above that of the ambient water (2-7). This "RM endothermy" (see SI Materials and Methods for terminology) in fishes represents a remarkable example of convergent evolution, because bony fishes and cartilaginous fishes diverged as long as 450 million years ago (8). In addition to elevated RM temperature, tunas and endothermic sharks share a number of morphological (e.g., medially located RM), physiological (e.g., high metabolic rates), and ecological (e.g., highly mobile and predatory lifestyle) characteristics (9).RM endothermy is an energetically expensive thermal strategy (9), and its convergent evolution indicates that the extra energetic costs incurred by RM endothermy can be outweighed by some ecological advantages. This topic has been discussed intensively, and two primary, nonmutually exclusive hypotheses have been proposed: expansion of the thermal niche and elevated cruising speeds (2). The thermal niche hypothesis states that fishes with RM endothermy can tolerate a broader range of water temperatures and, thus, can expand thei...

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“…2) and thunniform swimming mode (where lateral movements are largely confined to the caudal region) associated with a unique force-transmission system from RM to the caudal region (25).…”

Section: Resultsmentioning

confidence: 99%

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Watanabe

Goldman

Caselle

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

109

139

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“…In fact, kinematics, ground reaction force determination, or both have been used in a variety of species such as elephants [33][34][35] , cattle 36 , horses [37][38][39][40] , dogs 4,[41][42][43][44][45] , cats 21,[46][47][48][49] , various rodents 3,8,50,51 , birds 4,[52][53][54][55] , and fish 56,57 (this list is by no means exhaustive). In the authors' experience, however, the use of mice is problematic given that mice are not easy to operantly condition to travel along a runway.…”

Section: Discussionmentioning

confidence: 99%

Kinematics and Ground Reaction Force Determination: A Demonstration Quantifying Locomotor Abilities of Young Adult, Middle-aged, and Geriatric Rats

Webb

Kerr

Neville

et al. 2011

JoVE

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Behavior, in its broadest definition, can be defined as the motor manifestation of physiologic processes. As such, all behaviors manifest through the motor system. In the fields of neuroscience and orthopedics, locomotion is a commonly evaluated behavior for a variety of disease models. For example, locomotor recovery after traumatic injury to the nervous system is one of the most commonly evaluated behaviors [1][2][3] . Though locomotion can be evaluated using a variety of endpoint measurements (e.g. time taken to complete a locomotor task, etc), semiquantitative kinematic measures (e.g. ordinal rating scales (e.g. Basso Beattie and Bresnahan locomotor (BBB) rating scale, etc)) and surrogate measures of behaviour (e.g. muscle force, nerve conduction velocity, etc), only kinetics (force measurements) and kinematics (measurements of body segments in space) provide a detailed description of the strategy by which an animal is able to locomote 1 . Though not new, kinematic and kinetic measurements of locomoting rodents is now more readily accessible due to the availability of commercially available equipment designed for this purpose. Importantly, however, experimenters need to be very familiar with theory of biomechanical analyses and understand the benefits and limitations of these forms of analyses prior to embarking on what will become a relatively labor-intensive study. The present paper aims to describe a method for collecting kinematic and ground reaction force data using commercially available equipment. Details of equipment and apparatus set-up, pre-training of animals, inclusion and exclusion criteria of acceptable runs, and methods for collecting the data are described. We illustrate the utility of this behavioral analysis technique by describing the kinematics and kinetics of strain-matched young adult, middleaged, and geriatric rats.

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“…Recent examples include Donley et al's (2004) analysis of similar morphological and biomechanical specialisations in lamnid sharks and tuna, such as a "thunniform" body shape, in both cases caused by selection for fast movement through water. This convergent evolution (Endler's third method) has occurred independently during the 400 million years since the two groups diverged from a common ancestor.…”

Section: Experimental Population Geneticsmentioning

confidence: 99%

Towards a unified science of cultural evolution

2006

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We suggest that human culture exhibits key Darwinian evolutionary properties, and argue that the structure of a science of cultural evolution should share fundamental features with the structure of the science of biological evolution. This latter claim is tested by outlining the methods and approaches employed by the principal subdisciplines of evolutionary biology and assessing whether there is an existing or potential corresponding approach to the study of cultural evolution. Existing approaches within anthropology and archaeology demonstrate a good match with the macroevolutionary methods of systematics, paleobiology, and biogeography, whereas mathematical models derived from population genetics have been successfully developed to study cultural microevolution. Much potential exists for experimental simulations and field studies of cultural microevolution, where there are opportunities to borrow further methods and hypotheses from biology. Potential also exists for the cultural equivalent of molecular genetics in "social cognitive neuroscience," although many fundamental issues have yet to be resolved. It is argued that studying culture within a unifying evolutionary framework has the potential to integrate a number of separate disciplines within the social sciences.

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Convergent evolution in mechanical design of lamnid sharks and tunas

Cited by 141 publications

References 19 publications

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes

Kinematics and Ground Reaction Force Determination: A Demonstration Quantifying Locomotor Abilities of Young Adult, Middle-aged, and Geriatric Rats

Towards a unified science of cultural evolution

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