Natural and anthropogenic sources of habitat variation influence exploration behaviour, stress response, and brain morphology in a coastal fish

1. Evolutionary ecology aims to better understand how ecologically
important traits respond to environmental heterogeneity. Environments vary
both naturally and as a result of human activities, and investigations
that simultaneously consider how natural and human-induced environmental
variation affect diverse trait types grow increasingly important as human
activities drive species endangerment. 2. Here, we examine how habitat
fragmentation and structural habitat complexity, affect disparate trait
types in Bahamas mosquitofish (Gambusia hubbsi) inhabiting tidal creeks.
We tested a priori predictions for how these factors might influence
exploratory behaviour, stress reactivity, and brain anatomy. 3. We
examined approximately 350 adult Bahamas mosquitofish from seven tidal
creek populations across Andros Island, The Bahamas that varied in both
human-caused fragmentation (three fragmented, four unfragmented) and
natural habitat complexity (e.g. 5-fold variation in rock habitat). 4.
Populations that had experienced severe human-induced fragmentation, and
thus restriction of tidal exchange from the ocean, exhibited greater
exploration of a novel environment, stronger physiological stress
responses to a mildly stressful event, and smaller telencephala (relative
to body size). These changes matched adaptive predictions based mostly on
1) reduced chronic predation risk and 2) decreased demands for navigating
tidally dynamic habitats. Populations from sites with greater structural
habitat complexity showed a higher propensity for exploration and a
relatively larger optic tectum and cerebellum. These patterns matched
adaptive predictions related to increased demands for navigating complex
environments. 5. Our findings demonstrate environmental variation,
including recent anthropogenic impacts (<50 years), can
significantly affect complex, ecologically important traits. Yet
trait-specific patterns may not be easily predicted, as we found strong
support for only six of 12 predictions. Our results further highlight the
utility of simultaneously quantifying multiple environmental factors—e.g.
had we failed to account for habitat complexity, we would not have
detected effects of fragmentation on exploratory behaviours. These
responses, and their ecological consequences, may be complex: rapid and
adaptive phenotypic responses to anthropogenic impacts can facilitate
persistence in human-altered environments, but may come at a cost of
population vulnerability if ecological restoration were to occur without
consideration of the altered traits.

1. 进化生态学旨在深入解析生态重要性状如何响应环境异质性。环境的变化既源于自然过程，也受人类活动影响；随着人类活动加剧物种濒危危机，同时考量自然与人为环境变异对多种性状类型作用的研究，其重要性日益凸显。
2. 本研究以栖息于潮汐溪流的巴哈马食蚊鱼（Gambusia hubbsi）为对象，探究生境破碎化与生境结构复杂性对其多种不同性状类型的影响。我们针对这两类因子对探索行为、应激反应及脑解剖结构的作用，检验了先验预测假说。
3. 我们采集了巴哈马安德罗斯岛7个潮汐溪流种群的约350尾成体巴哈马食蚊鱼；这些种群在人为造成的生境破碎化（3个破碎化种群、4个非破碎化种群）与自然生境结构复杂性（例如岩石生境差异达5倍）方面均存在变异。
4. 经历过严重人为破碎化（进而阻断了海洋潮汐交换）的种群，对新环境的探索程度更高、对轻度应激事件的生理应激反应更强，且端脑体积相对于体尺更小。这些变化主要符合两项适应性预测：一是长期捕食风险降低，二是潮汐动态生境的导航需求下降。而生境结构复杂性更高的种群，其探索倾向更强，视顶盖与小脑的相对体积也更大。这些模式同样符合与复杂生境导航需求提升相关的适应性预测。
5. 本研究结果表明，包括近50年来的人为活动影响在内的环境变异，可显著影响复杂的生态重要性状。但性状特异性的变化模式未必易于预测——本研究仅在12项预测中得到6项的强力支持。我们的结果进一步凸显了同时量化多种环境因子的必要性：例如，若未考量生境结构复杂性，我们将无法检测到生境破碎化对探索行为的影响。这些响应及其生态后果可能极为复杂：针对人为活动影响的快速适应性表型响应，可帮助物种在人类改造的生境中存续，但如果开展生态修复时未考虑这些已发生改变的性状，种群可能因此面临更高的脆弱性风险。