Divergent Behavior Amid Convergent Evolution: A Case of Four Desert Rodents Learning to Respond to Known and Novel Vipers

Abstract

14Desert communities word-wide are used as natural laboratories for the study of convergent 15 evolution, yet inferences drawn from such studies are necessarily indirect. Here, we brought 16 desert organisms together (rodents and vipers) from two deserts (Mojave and Negev). Both 17 predators and prey in the Mojave have adaptations that give them competitive advantage 18 compared to their middle-eastern counterparts. Heteromyid rodents, kangaroo rats and pocket 19 mice, have fur-lined cheek pouches that allow the rodents to carry larger loads under predation 20 risk compared to gerbilline rodents. Sidewinder rattlesnakes have heat-sensing pits, allowing 21 them to hunt better on moonless nights when their Negev sidewinding counterpart, the Saharan 22 horned vipers, are visually impaired. In behavioral-assays, we used giving-up density (GUD) to 23 gage how each species of rodent perceived risk posed by known and novel snakes. We repeated 24 this for the same set of rodents at first encounter and again two months later following intensive 25 "natural" exposure to both snake species. Pre-exposure, all rodents identified their evolutionarily 26 familiar snake as a greater risk than the novel one. However, post-exposure all identified the 27 heat-sensing sidewinder rattlesnake as a greater risk. The heteromyids were more likely to avoid 28 encounters with, and discern the behavioral difference among, snakes than their gerbilline 29 counterparts. 30 31 34Deserts, and desert rodents in particular, provide a model system for studying parallel and 35 convergent evolution. Deserts around the world form at least five evolutionarily independent 36 laboratories of adaptation, ecology, and evolution [1][2][3][4][5][6]. Shared environmental conditions of 37 temperature, precipitation, and aridity force evolutionary processes in a manner that results in 38 similar adaptations in species that fill similar ecological roles. Not only do species converge, but 39 communities may too [7][8][9][10]. A good example of this can be studied in desert dunes of the 40 Mojave and of the Negev deserts. In both of these systems we find an array of plants that drop 41 their seeds onto the sand (creating a seed bank); a variety of rodent species feed on these seeds 42 [11][12][13]; and medium-sized sidewinding vipers feed on the rodents [14,15]. 43The Mojave and Negev deserts of North America and the Middle East, respectively, 44 possess rodents with similar ecologies [5,7,13,16,17]. These rodents are nocturnal, semi-45 fossorial, seed-eating, and seed caching. However, the heteromyid rodents of the Mojave may 46 have a constraint breaking adaptation compared to their convergent counterparts in the Negev, 47 the gerbilline rodents. A constraint-breaking adaptation is a game-changing evolutionary 48 adaptation that alters, relaxes or eliminates tradeoffs and confers a competitive advantage to its 49 holder over those lacking the trait as defined by Rosenzweig and McCord [18]. The heteromyids 50 have external fur lined cheek pouches that allow...

Comparing Plasticity of Response to Perceived Risk in the Textbook Example of Convergent Evolution of Desert Rodents and Their Predators; a Manipulative Study Employing the Landscape of Fear

“…The model also found a significant difference among species’ foraging tenacity and for each species an interaction of owl presence with microhabitat and owl presence with snake treatment (quadrant). We do not offer in-depth examination here of these differences as they distract from the main purpose of this article, and are the basis for a number of articles published separately (Bleicher, 2014; Bleicher et al, 2016, 2018a; Kotler et al, 2016).…”

“…In that experiment, which was run first and acted as a pilot, we tested two additional layers of complexity not tested in the other species. We ran four six-night rounds per month centered around each of the four moonphases (new, waxing, full, waning), with only two nights per moonphase with the owls (Bleicher, 2014; Bleicher et al, 2016). Additionally, the experiment also added rotations with a muzzled red fox for two nights per moonphase.…”

Balancing food, activity and the dangers of sunlit nights

“…From other experiments, we find evidence that use of bioassays to measure animal behavior will always be associated with extra stress. Taking animals out of their holding pens and transferring them into a novel and sterile environment will at the minimum produce neophobia (Bolbroe et al 2000) and at more extreme cases even cause animals to cease activity all together (Bleicher et al 2018a).…”

Camouflage in arid environments: the case of Sahara-Sahel desert rodents

“…They are harsh environments, severely limited by annual precipitation (Holt et al 2013, Vale & Brito 2015, and therefore, desert organisms have been studied from the perspective of adaptation to arid conditions ). Due to a lack of vegetation (or surface structures), exposed desert habitats provide an opportunity to understand natural selection under extreme conditions (Dice 1947, Nachman et al 2003, Hoekstra et al 2006, Boratyński et al 2014, Bleicher et al 2018.…”

“…In this process, natural sorting of the genetic constituents of Camouflage in arid environments: the case of Sahara-Sahel desert rodents individuals at the phenotypic level occurs (Reznick 2016). Selection can shape phenotypic variation due to covariation, for example, between prey phenotypic features and predation pressure, as in desert rodents , Hoekstra et al 2006, Boratyński et al 2017, Bleicher et al 2018. Therefore, predator-induced selection can drive evolution of prey anti-predatory adaptations, such as high mobility and saltation behaviour (Alhajeri 2016), bullar hypertrophy (i.e.…”