Earth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada.
Department of Biology and Marine Biology, University of North Carolina, Wilmington, North Carolina, USA.
J Fish Biol. 2021 Sep;99(3):990-998. doi: 10.1111/jfb.14797. Epub 2021 Jun 11.
Brain size varies dramatically, both within and across species, and this variation is often believed to be the result of trade-offs between the cognitive benefits of having a large brain for a given body size and the energetic cost of sustaining neural tissue. One potential consequence of having a large brain is that organisms must also meet the associated high energetic demands. Thus, a key question is whether metabolic rate correlates with brain size. However, using metabolic rate to measure energetic demand yields a relatively instantaneous and dynamic measure of energy turnover, which is incompatible with the longer evolutionary timescale of changes in brain size within and across species. Morphological traits associated with oxygen consumption, specifically gill surface area, have been shown to be correlates of oxygen demand and energy use, and thus may serve as integrated correlates of these processes, allowing us to assess whether evolutionary changes in brain size correlate with changes in longer-term oxygen demand and energy use. We tested how brain size relates to gill surface area in the blacktip shark Carcharhinus limbatus. First, we examined whether the allometric slope of brain mass (i.e., the rate that brain mass changes with body mass) is lower than the allometric slope of gill surface area across ontogeny. Second, we tested whether gill surface area explains variation in brain mass, after accounting for the effects of body mass on brain mass. We found that brain mass and gill surface area both had positive allometric slopes, with larger individuals having both larger brains and larger gill surface areas compared to smaller individuals. However, the allometric slope of brain mass was lower than the allometric slope of gill surface area, consistent with our prediction that the allometric slope of gill surface area could pose an upper limit to the allometric slope of brain mass. Finally, after accounting for body mass, individuals with larger brains tended to have larger gill surface areas. Together, our results provide clues as to how fishes may evolve and maintain large brains despite their high energetic cost, suggesting that C. limbatus individuals with a large gill surface area for their body mass may be able to support a higher energetic turnover, and, in turn, a larger brain for their body mass.
大脑大小在物种内和物种间都有很大的差异，这种差异通常被认为是大脑大小与身体大小的认知益处之间权衡的结果，以及维持神经组织的能量成本。拥有一个大的大脑的一个潜在后果是，生物体还必须满足相关的高能量需求。因此，一个关键的问题是代谢率是否与大脑大小相关。然而，使用代谢率来衡量能量需求会得到一个相对瞬时和动态的能量转换测量，这与物种内和物种间大脑大小变化的更长进化时间尺度不兼容。与耗氧量相关的形态特征，特别是鳃表面积，已被证明与氧需求和能量利用有关，因此可能是这些过程的综合相关物，使我们能够评估大脑大小的进化变化是否与长期的氧需求和能量利用变化相关。我们测试了黑鳍鲨 Carcharhinus limbatus 的大脑大小与鳃表面积的关系。首先，我们检查了大脑质量的异速生长斜率（即大脑质量随体重变化的速率）是否低于个体发育过程中鳃表面积的异速生长斜率。其次，我们测试了在考虑体重对大脑质量的影响后，鳃表面积是否能解释大脑质量的变化。我们发现大脑质量和鳃表面积都有正异速生长斜率，与较小个体相比，较大个体既有更大的大脑，也有更大的鳃表面积。然而，大脑质量的异速生长斜率低于鳃表面积的异速生长斜率，这与我们的预测一致，即鳃表面积的异速生长斜率可能对大脑质量的异速生长斜率构成上限。最后，在考虑体重后，大脑较大的个体往往具有较大的鳃表面积。总的来说，我们的研究结果为鱼类如何在高能量成本的情况下进化和维持大脑提供了线索，表明具有与其体重相匹配的较大鳃表面积的 C. limbatus 个体可能能够支持更高的能量转换，从而为其体重提供更大的大脑。
