Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche

Abstract

31Adaptation to novel ecological niches often includes shifts in behaviors, such as new foraging 32 preferences or changes in kinematics. Investigating prey capture kinematics is an excellent way 33 to understand behavioral mechanisms underlying the origins of novel trophic specialization, in 34 which organisms begin to exploit novel resources. We investigated the contribution of 35 kinematics to the origins of a novel ecological niche for scale-eating within a microendemic 36 adaptive radiation of pupfishes on San Salvador Island, Bahamas. We compared the feeding 37 kinematics of scale-eating, generalist, snail-eating, and F1 hybrid pupfishes while they consumed 38 scales and shrimp in the lab and compared them to scale-eating kinematics observed in situ in the 39 wild. We then connected variation in feeding kinematics to scale-biting performance by 40 measuring the area removed per strike from standardized gelatin cubes. We found that scale-41 eating pupfish exhibited divergent feeding kinematics compared to all other groups and that 42 these differences were consistent across food items. The peak gapes of scale-eaters were twice as 43 large as all other groups, but their gape angles were simultaneously 32% smaller, in both 44 laboratory and in situ wild observations. We also show that this kinematic combination of large 45 peak gape and small gape angle resides on a performance optimum for scale-biting. Finally, F1 46 hybrid kinematics and performance were not additive, and were instead closer to the generalist 47 pupfish. This suggests that impaired hybrid performance in the scale-eating niche may contribute 48 to extrinsic postzygotic reproductive isolation between species. Ultimately, our results suggest 49 that shifts in kinematics (i.e. peak gape and gape angle) are an adaptation to the novel niche of 50 scale-eating and contribute to reproductive isolation between species. 51 52

How to Investigate the Origins of Novelty: Insights Gained from Genetic, Behavioral, and Fitness Perspectives

“…Over 50% of the diet of the scale-eating pupfish results from high-speed (10–15 ms) strikes biting scales and protein-rich mucus from other fishes, usually generalist pupfish which make up 95% of the fish community ( Martin and Wainwright 2013a ; McLean and Lonzarich 2017 ; St. John and Martin 2019 ). This specialized niche has evolved more than 19 times in fishes across diverse environments from the deep sea ( Nakae and Sasaki 2002 ) to the Amazon basin ( Evans et al.…”

“…This is particularly striking given that scale-eating involves high-speed ramming strikes on pupfish prey, an escalation of typical aggressive behavior, whereas consuming snails does not require high-speed strikes nor conspecific aggression, only increased stability of oral and pharyngeal jaws ( Hernandez et al. 2017 ; St. John and Martin 2019 ). These results do not support the aggression hypothesis and indicate that both specialists may exhibit high levels of aggression due to trophic specialization or due to the indirect effects of selection on other traits ( St. John et al.…”

“…Further investigation of the relative isolation of performance optima through biomechanical and kinematic models ( Holzman et al. 2012 ; Tseng 2013 ; Stayton 2019 ; St. John and Martin 2019 ) and fitness optima, particularly in natural field environments ( Keagy et al. 2016 ; Pfaender et al.…”

Hybridization alters the shape of the genotypic fitness landscape, increasing access to novel fitness peaks during adaptive radiation

“…Found in the benthic littoral zone of each lake, all three species forage within the same benthic microhabitat; indeed, no habitat segregation has been observed in 14 years of field studies. Originating less than 10,000 years ago (based on geological age estimates for the lakes: (49)), the functional and trophic novelty harbored within this radiation is the product of exceptional rates of craniofacial morphological evolution (50–53). Furthermore, species boundaries persist across multiple lake populations, despite persistent admixture among species (54, 55).…”

Ecological adaptation of an F1 hybrid cross of carnivorous and herbivorous Cyprinidae fishes

“…Some researchers thought that hybridization was an evolutionary dead end [1], because hybrids were more often observed to be less healthy and ecologically adapted than either parent species, and tended to be sterile [2][3][4][5][6][7]. However, others indicated that hybridization can provide an important source of genetic variation on which selection might act and that its adaptive role was more widespread [8][9][10][11][12][13][14][15][16]. The survival and adaptation of F1 hybrids is the first and most important step in hybrid speciation and is affected by both genetic and ecological challenges.…”