The findings from our study contribute significant insights into the intricate evolution of coloration among Sphenarium grasshopper species. The observed disparities in color patterns among these species are attributed to localized adaptations to distinct environmental conditions. It is evident that natural selection has favoured the development of cryptic coloration in both male and female grasshoppers. However, a nuanced gender-specific divergence is discernible in their responses to environmental cues. Notably, the brightness of males exhibits a positive correlation with the wettest trimester of the year, while the brightness and saturation of females are positively associated with the driest trimester. Intriguingly, despite the absence of direct correlations with climatic variables, female mark patterns demonstrate a positive connection with their backgrounds. Conversely, male patterns show no such relationship with their surroundings, although a significant link between male marks (overall pattern contrast) and the driest trimester is evident. An interesting aspect that emerges is the relatively rapid evolution of chromatic patterns compared to the evolution of marking patterns.
The disparity in the pace of evolutionary divergence between background resemblance and disruptive markings can be rationalized by the varied payoffs associated with each strategy. In scenarios where a species colonizes a new, vibrant, and uniform environment, natural selection tends to hasten the convergence of coloration with the new environment (referred to as BM). Conversely, the adaptability inherent in disruptive markings allows for a reduced divergence among species that face novel environments or alterations in their distribution range. In this context, the chromatic patterns exhibited by Sphenarium grasshoppers may embody a generalized strategy that moderately matches various backgrounds without precisely mimicking anyone. It's worth noting that the benefits derived from cryptic strategies differ between males and females. The divergence rate of hue1, overall pattern contrast, and dominant marking size are notably higher in males than in females. Conversely, the evolution of pattern diversity has proceeded independently within both genders, indicating a distinct niche specialization concerning light and shadow contrast for males and females. Nonetheless, the parallel evolution rates of brightness, saturation, and hue2 in males and females can be attributed to similar selective pressures faced by different species within their respective habitats.
The divergence in chromatic patterns within Sphenarium grasshoppers finds its basis in the diverse environments where the genus has diversified (as evidenced by Sanabria-Urbán et al. 2017) and the behavioural disparities between males and females. The synchronization of Sphenarium life cycles with rainy seasons, as discussed by Sanabria-Urbán et al. (2015), likely underlies the strong associations between chromatic patterns and environmental conditions exhibited across all species. This linkage is attributable to the profound influence of precipitation on primary productivity (Yom-Tov and Geffen 2006), resulting in alterations in vegetation color and shadow patterns. Furthermore, the variations in male and female populations due to precipitation fluctuations on different timescales are notable. For instance, the protandrous nature of males in certain species aligns their maturation with the onset of the rainy season, maximizing mating opportunities. During this phase, male brightness synchronizes with light-green shades, and their marks may serve them well during the subsequent driest trimester, characterized by deeper contrasts between light and shadow. In contrast, females, strategically maturing later than males, exhibit color and mark patterns that correlate with vegetation plots and backgrounds, which they frequent during their reproductive season.
Males' active pursuit of females, often atop plants, juxtaposes the stationary female behaviour, placing them closer to the ground where they lay eggs. The pattern of marks on the dorsal surface of these grasshoppers serves dual purposes, providing BM and potentially contributing to DC, as postulated by Robledo-Ospina et al. (2017). Such highly contrasting markings might disrupt predators' visual perception or divert attention from the organism's contours, an adaptive advantage, as Merilaita (1998) and Hughes et al. (2019) suggested. However, the potential implications of these marking patterns on processes such as sexual selection warrant consideration (with reference to Cueva del Castillo and Cano-Santana 2001). Notably, the divergence rate in male marking patterns surpasses that of females, indicating heightened natural selection pressure on these male-specific traits. Remarkably, in the case of S. zapotecum, predators allocate more time to locate striped male morphs with reduced BM and increased disruptive characteristics and females with heightened background resemblance. This behaviour augments prey survival (Ramírez-Delgado and Cueva del Castillo 2023).
It is conceivable that these grasshoppers adopt a form of camouflage that offers partial resemblance to multiple backgrounds rather than a perfect match to a singular habitat. Alternatively, their camouflage may operate somewhat autonomously from BM strategies (as posited by Hughes et al. 2019). Nevertheless, the apparent convergence between Sphenarium chromatic patterns and their environments stems from a blend of differential predation dynamics and proactive habitat selection. This phenomenon parallels other grasshopper species (as demonstrated by Edelaar et al. 2017, 2019; Heinze et al. 2022).
The survival of these grasshoppers hinges on their ability to navigate diverse predator threats, including avian, mammalian, reptilian, and arthropod predators (Kevan 1977), as well as human predation (highlighted by Sanabria-Urbán and Cueva del Castillo 2020). Their chromatic and achromatic visual cues have evolved in response to the distinct searching strategies of these predators. Remarkably, the resemblance of marking patterns to the environment extends to chromatic and achromatic variables. However, while chromatic cues excel in close-range searches, achromatic information proves more effective in long-distance prey detection (Schaefer and Stobbe 2006; Cazetta et al. 2009). Notably, human behaviour as a predator mirror that of natural predators, particularly birds, a similarity exploited in some studies to predict predation by other visual predators in natural settings (Karpestam et al. 2013). This intriguing correspondence has likely influenced the evolution of Sphenarium grasshoppers' chromatic patterns.
Considering the relative scarcity of phylogenetic comparative studies concerning cryptic coloration evolution, our research undoubtedly contributes to a foundational comprehension of color evolution within the context of selection pressures imposed by visual predators. Nonetheless, it is imperative to acknowledge that future investigations into habitat preference and the exploration of other potential functions of grasshopper coloration, such as thermoregulation or UV radiation protection, hold the potential to unveil additional factors shaping the evolution of coloration within this cohort of neotropical grasshoppers.