Evolutionary trade-offs may interact with physiological constraints to maintain color variation

Animal coloration is a multifaceted trait with many ecological roles and
related to a variety of developmental and physiological processes.
Consequently, coloration is often subject to a variety of selective
pressures, leading to the evolutionary maintenance of variation. In this
study, we investigated hypotheses related to the maintenance of dorsal
color variation in wood frogs (Rana sylvatica). First, we tested for
multimodality, and whether color correlates with body size or condition or
varies by sex or age-class. We combined behavioral trials with visual
modeling to test for sex recognition. We also considered visual models for
predators and tested for an interaction between discriminability indexes
(JND) of color channel (chromatic vs. achromatic) and predator type (birds
vs. snakes), as well as for a within individual trade-off between the JND
of chromatic and achromatic coloration. Finally, we tested for disruptive
viability selection on color using predation trials, and for antagonistic
directional selection between viability selection and reproductive
investment of females. We found that wood frogs present continuous color
variation that does not correlate with body size or condition, but that
changes with age. Wood frogs present subtle sexual dichromatism, but we
found no evidence for a role of color in sex recognition. Instead, we
discuss the possibility that sex differences might, at least in part, have
a demographic explanation. Predator visual models indicated that wood
frogs cannot solely rely on dorsal coloration for camouflage. Moreover,
different predators might present selective pressures in different color
channels, while individuals’ achromatic and chromatic coloration trade-off
in JND. Therefore, different selective pressures caused by different
predators might interact with ontogenetic changes and
developmental/physiological trade-offs to maintain color variation. We
found no relationship between color and survival or reproductive
investment, suggesting further work is required to fully understand
selection on color. Our results highlight the importance of understanding
evolutionary trade-offs and developmental/physiological constraints in
combination with one another, and suggest the potential for an interaction
between these proximate and ultimate mechanisms in the evolutionary
maintenance of variation. These results likely extend beyond color
expression in amphibians, and exemplify a more general process for such
evolutionary outcomes.

动物体色是一类兼具多重生态功能的多维度性状，且与多种发育及生理过程密切相关。因此，体色常受到多种选择压力的作用，进而推动了变异的进化维持。本研究针对林蛙（Rana sylvatica）背部颜色变异的维持机制展开了相关假说验证：首先，我们检验了体色变异的多峰性，以及体色是否与体型、身体状况相关，或因性别、年龄组而异；其次，我们结合行为实验与视觉建模方法，对性别识别相关的体色作用进行了检验；此外，我们还构建了捕食者的视觉模型，检验了颜色通道（色觉通道与非色觉通道）的可察觉差异指数（JND）与捕食者类型（鸟类与蛇类）之间的交互效应，以及个体内部色觉与非色觉体色可察觉差异之间的权衡关系；最后，我们通过捕食实验检验了体色上的破坏性存活选择，并检验了雌性个体存活选择与繁殖投入之间的拮抗定向选择。研究结果显示，林蛙的体色变异呈连续分布，且与体型、身体状况无显著关联，但随年龄增长发生变化。林蛙存在微弱的性别二态体色，但我们未发现体色在性别识别中发挥作用的证据，对此我们提出一种可能性：性别体色差异至少部分可通过种群统计学机制进行解释。捕食者视觉模型结果表明，林蛙无法仅依靠背部体色实现伪装。此外，不同捕食者可能对不同颜色通道施加差异化的选择压力，而个体的非色觉与色觉体色在可察觉差异上存在权衡。因此，不同捕食者带来的差异化选择压力，可能与个体发育变化、发育/生理权衡共同作用，进而维持体色变异。我们未发现体色与存活率或繁殖投入之间存在关联，这表明未来仍需开展更多研究以全面解析体色所受的选择作用。本研究结果凸显了整合解析进化权衡与发育/生理约束的重要性，并暗示这些近因机制与终极机制之间的交互作用，可能在变异的进化维持中发挥关键作用。上述研究结论不仅适用于两栖动物的体色表达，也为这类进化结果提供了更具普适性的过程范例。