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Potential Enhanced Ability of Giant Squid to Detect Sperm Whales Is an Exaptation Tied to Their Large Body Size

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Potential Enhanced Ability of Giant Squid to Detect Sperm Whales Is an Exaptation Tied to Their Large Body Size UC Davis UC Davis Previously Published Works Title Potential enhanced ability of giant squid to detect sperm whales is an exaptation tied to their large body size Permalink https://escholarship.org/uc/item/0730p988 Journal BMC Evolutionary Biology, 13(1) ISSN 1471-2148 Authors Schmitz, Lars Motani, Ryosuke Oufiero, Christopher E et al. Publication Date 2013-10-15 DOI http://dx.doi.org/10.1186/1471-2148-13-226 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Schmitz et al. BMC Evolutionary Biology 2013, 13:226 http://www.biomedcentral.com/1471-2148/13/226 CORRESPONDENCE Open Access Potential enhanced ability of giant squid to detect sperm whales is an exaptation tied to their large body size Lars Schmitz1*, Ryosuke Motani2, Christopher E Oufiero3, Christopher H Martin4, Matthew D McGee5 and Peter C Wainwright5 Abstract It has been hypothesized that sperm whale predation is the driver of eye size evolution in giant squid. Given that the eyes of giant squid have the size expected for a squid this big, it is likely that any enhanced ability of giant squid to detect whales is an exaptation tied to their body size. Future studies should target the mechanism behind the evolution of large body size, not eye size. Reconstructions of the evolutionary history of selective regime, eye size, optical performance, and body size will improve the understanding of the evolution of large eyes in large ocean animals. Keywords: Giant squid, Sperm whale, Eye size, Optical function, Scaling, Allometry, Adaptation, Exaptation Introduction whales. In our paper [2] we further explored this adap- The giant squid is an increasingly popular species for tive hypothesis and provided comparative eye size data examining the optical functions and evolutionary drivers for squid and a re-parameterization of Nilsson et al.’s of large eyes in deep sea animals, with a series of papers model that casted doubt on swimming sperm whale pre- published within the last 2 years [1-3]. Nilsson and col- dation driving giant squid eye evolution. The current leagues [1] recently commented on a paper in which we contribution of Nilsson and colleagues [1] does not re- explored the scaling relations of body and eye size in fute our data or observations. As we outline below, cen- squid [2]. Our paper [2] itself was inspired by previous tral to this interesting discussion is the methodological work of Nilsson and colleagues [3] who developed a approach for testing adaptive hypotheses in evolutionary functional model that allows exploration of vision in the morphology. deep sea. This model represented a major creative break- through in the field of animal sensory biology, without Discussion doubt paving the way for many future studies. Nilsson Adaptations are traits that improve evolutionary fitness, and colleagues introduced their new model with a case originally shaped by natural selection for their current study on giant squid, one of the most enigmatic and role [4]. Thorough tests of adaptive hypotheses require charismatic animals populating the oceans today. Giant the integration of multiple lines of evidence [5,6]. A con- squid are elusive and thus very poorly known, yet optical vincing phylogenetic argument for the case of an adapta- modeling may indirectly illuminate some aspects of their tion is achieved when selective regime, trait, and functional biology. Nilsson and colleagues concluded [3] that the capacity of the trait evolve concordantly. When applied evolution of giant eyes may have been driven by preda- to the giant squid problem the following questions need tion, because very large eyes seemed uniquely suited for to be addressed: a) when (i.e., along which lineages) did detecting large, approaching predators such as sperm squid invade the mesopelagic realm and experienced pre- dation from large oceanic predators?; b) when did relative * Correspondence: [email protected] eye size change?; and c) when did visual performance 1W.M. Keck Science Department, Claremont McKenna College, Pitzer College, and Scripps College, Claremont, CA 91711, USA change? Given that sperm whales feed on many squid Full list of author information is available at the end of the article species other than giant and colossal squid [2], one would © 2013 Schmitz et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Schmitz et al. BMC Evolutionary Biology 2013, 13:226 Page 2 of 3 http://www.biomedcentral.com/1471-2148/13/226 expect adaptive increases in eye size in several indepen- of a ‘law of diminishing returns’ but caution to interpret dent lineages. the presence of negative allometry as sufficient evidence. Nilsson and colleagues provided an important piece to Eyes of both terrestrial and marine vertebrates scale with the puzzle in their original paper [3]: the modeling of negative allometry and this observation has been linked to functional capability of eyes depending on their size and the scaling of brains [7]. It will be difficult to test this hy- the physical characteristics of the environments in which pothesis as there are many possible competing explana- eyes operate. However, the phylogenetic lines of evi- tions for the observed pattern, but we hope this question dence that are necessary to make a strong case for adap- will be addressed in future studies. tation are missing. The development of a functional 2. On the second issue, in the present contribution mechanism by itself, even though important, is insuffi- Nilsson and colleagues build upon our re-parameterization cient to support evolutionary adaptations. of the original parameterization of their model by adding In our paper [2] we revisited the conclusions of Nilsson a new element. In doing so they reinstated their original and colleagues in order to better understand the possible conclusion that giant squid eyes are unusually good at adaptive significance of giant squid eyes. Our paper was seeing the glow of bioluminescence produced by swim- not designed as a comprehensive test of the adaptive hy- ming sperm whales. However, it seems somewhat optimis- pothesis but provided the much needed benefit of (1) a tic to move forward as though the giant squid problem is new data set on the scaling of squid eye diameter that resolved with a third parameterization of the model. It has places the relative eye size of giant squid in a comparative become clear that the results of the model and the impli- context and (2) some reconsideration of the values Nilsson cations are very sensitive to parameters used in the model and colleagues used to parameterize their model. Our work and there will always be room for improvement. The new led to two points where we differ with the conclusions of element in the model, an estimate of displaced water vo- Nilsson and colleagues, concerning whether giant and lume in which bioluminescence is triggered, is not exempt colossal squid have exceptionally large eyes and whether from this, especially given that it is not backed up by com- the model results were consistent with a unique func- putational or experimental evidence. That being said, we tional advantage to those large eyes. strongly agree that these squid must sometimes be able to 1. On the first issue, we found the diameter of giant see the bioluminescence caused by swimming sperm and colossal squid eyes fall within 95% prediction inter- whales. We also agree that big eyes improve performance vals on the basis of our data from 87 smaller squid spe- in this task. Indeed, in our paper we emphasized that cies. Our data show that giant and colossal squid eyes there are many benefits of large eyes to the visual per- are not unusually large for squid of their body size. Our formance of giant squid. conclusion was thus different from that of Nilsson and colleagues who wrote in their Current Biology paper Conclusions (penultimate paragraph of page 685): “Although other Where does this leave us in the discussion of eye size squid species generally have large eyes for their body evolution in giant squid? Enhanced light capture is a size, the allometric growth factor for smaller squid is functional consequence of large eyes, but not neces- below 0.7 [26], making the eyes of giant and colossal sarily the “explanation” for large eyes that Nilsson squid unusually large even for squid.” Our data indicate and colleagues argue they have provided. We believe that that this last statement is incorrect. Yet, in the current here lies the core issue in this discussion. As outlined contribution [1] Nilsson and colleagues again conclude above, the bar for a convincing adaptive argument of that “the giant eyes of giant squid are indeed unexpec- large eyes is much higher than showing how the structure tedly large” (from the title of their work). It appears the functions. discussion has become a semantic argument around Indeed, the simplest interpretation of the available data what is meant by ‘unexpectedly large’. Our data show actually is that any enhanced ability of these squids to that giant and colossal squid are large squid whose eye detect whales is an exaptation tied to their large body size follows the scaling pattern between body size and size – a performance trait that was carried along with eye size in other squid. They do not have unexpectedly the evolution of large body size. Most of the difference large eyes for their body size.
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