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Building trophic specializations that result in substantial niche partitioning within a young adaptive radiation

(2018) JOURNAL OF ANATOMY. 232(2). p.173-185
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Abstract
Dietary partitioning often accompanies the increased morphological diversity seen during adaptive radiations within aquatic systems. While such niche partitioning would be expected in older radiations, it is unclear how significant morphological divergence occurs within a shorter time period. Here we show how differential growth in key elements of the feeding mechanism can bring about pronounced functional differences among closely related species. An incredibly young adaptive radiation of three Cyprinodon species residing within hypersaline lakes in San Salvador Island, Bahamas, has recently been described. Characterized by distinct head shapes, gut content analyses revealed three discrete feeding modes in these species: basal detritivory as well as derived durophagy and lepidophagy (scale-feeding). We dissected, cleared and stained, and micro-CT scanned species to assess functionally relevant differences in craniofacial musculoskeletal elements. The widespread feeding mode previously described for cyprinodontiforms, in which the force of the bite may be secondary to the requisite dexterity needed to pick at food items, is modified within both the scale specialist and the durophagous species. While the scale specialist has greatly emphasized maxillary retraction, using it to overcome the poor mechanical advantage associated with scaleeating, the durophage has instead stabilized the maxilla. In all species the bulk of the adductor musculature is composed of AM A1. However, the combined masses of both adductor mandibulae (AM) A1 and A3 in the scale specialist were five times that of the other species, showing the importance of growth in functional divergence. The scale specialist combines plesiomorphic jaw mechanisms with both a hypertrophied AM A1 and a slightly modified maxillary anatomy (with substantial functional implications) to generate a bite that is both strong and allows a wide range of motion in the upper jaw, two attributes that normally tradeoff mechanically. Thus, a significant feeding innovation (scale-eating, rarely seen in fishes) may evolve based largely on allometric changes in ancestral structures. Alternatively, the durophage shows reduced growth with foreshortened jaws that are stabilized by an immobile maxilla. Overall, scale specialists showed the most divergent morphology, suggesting that selection for scale-biting might be stronger or act on a greater number of traits than selection for either detritivory or durophagy. The scale specialist has colonized an adaptive peak that few lineages have climbed. Thus, heterochronic changes in growth can quickly produce functionally relevant change among closely related species.
Keywords
adductor mandibulae, Cyprinodon, durophagy, functional morphology, jaw, lepidophagy, scale-eating, REMARKABLE SPECIES FLOCK, SAN-SALVADOR ISLAND, CYPRINODONTIFORM FISHES, EVOLUTIONARY NOVELTY, PUPFISHES, MECHANISM, DIVERSIFICATION, TELEOSTEI, RATES, POPULATIONS

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Citation

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Chicago
Hernandez, Luz Patricia, Dominique Adriaens, Christopher H Martin, Peter C Wainwright, Bert Masschaele, and Manuel Dierick. 2018. “Building Trophic Specializations That Result in Substantial Niche Partitioning Within a Young Adaptive Radiation.” Journal of Anatomy 232 (2): 173–185.
APA
Hernandez, L. P., Adriaens, D., Martin, C. H., Wainwright, P. C., Masschaele, B., & Dierick, M. (2018). Building trophic specializations that result in substantial niche partitioning within a young adaptive radiation. JOURNAL OF ANATOMY, 232(2), 173–185.
Vancouver
1.
Hernandez LP, Adriaens D, Martin CH, Wainwright PC, Masschaele B, Dierick M. Building trophic specializations that result in substantial niche partitioning within a young adaptive radiation. JOURNAL OF ANATOMY. 2018;232(2):173–85.
MLA
Hernandez, Luz Patricia, Dominique Adriaens, Christopher H Martin, et al. “Building Trophic Specializations That Result in Substantial Niche Partitioning Within a Young Adaptive Radiation.” JOURNAL OF ANATOMY 232.2 (2018): 173–185. Print.
@article{8538488,
  abstract     = {Dietary partitioning often accompanies the increased morphological diversity seen during adaptive radiations within aquatic systems. While such niche partitioning would be expected in older radiations, it is unclear how significant morphological divergence occurs within a shorter time period. Here we show how differential growth in key elements of the feeding mechanism can bring about pronounced functional differences among closely related species. An incredibly young adaptive radiation of three Cyprinodon species residing within hypersaline lakes in San Salvador Island, Bahamas, has recently been described. Characterized by distinct head shapes, gut content analyses revealed three discrete feeding modes in these species: basal detritivory as well as derived durophagy and lepidophagy (scale-feeding). We dissected, cleared and stained, and micro-CT scanned species to assess functionally relevant differences in craniofacial musculoskeletal elements. The widespread feeding mode previously described for cyprinodontiforms, in which the force of the bite may be secondary to the requisite dexterity needed to pick at food items, is modified within both the scale specialist and the durophagous species. While the scale specialist has greatly emphasized maxillary retraction, using it to overcome the poor mechanical advantage associated with scaleeating, the durophage has instead stabilized the maxilla. In all species the bulk of the adductor musculature is composed of AM A1. However, the combined masses of both adductor mandibulae (AM) A1 and A3 in the scale specialist were five times that of the other species, showing the importance of growth in functional divergence. The scale specialist combines plesiomorphic jaw mechanisms with both a hypertrophied AM A1 and a slightly modified maxillary anatomy (with substantial functional implications) to generate a bite that is both strong and allows a wide range of motion in the upper jaw, two attributes that normally tradeoff mechanically. Thus, a significant feeding innovation (scale-eating, rarely seen in fishes) may evolve based largely on allometric changes in ancestral structures. Alternatively, the durophage shows reduced growth with foreshortened jaws that are stabilized by an immobile maxilla. Overall, scale specialists showed the most divergent morphology, suggesting that selection for scale-biting might be stronger or act on a greater number of traits than selection for either detritivory or durophagy. The scale specialist has colonized an adaptive peak that few lineages have climbed. Thus, heterochronic changes in growth can quickly produce functionally relevant change among closely related species.},
  author       = {Hernandez, Luz Patricia and Adriaens, Dominique and Martin, Christopher H and Wainwright, Peter C and Masschaele, Bert and Dierick, Manuel},
  issn         = {0021-8782},
  journal      = {JOURNAL OF ANATOMY},
  keyword      = {adductor mandibulae,Cyprinodon,durophagy,functional morphology,jaw,lepidophagy,scale-eating,REMARKABLE SPECIES FLOCK,SAN-SALVADOR ISLAND,CYPRINODONTIFORM FISHES,EVOLUTIONARY NOVELTY,PUPFISHES,MECHANISM,DIVERSIFICATION,TELEOSTEI,RATES,POPULATIONS},
  language     = {eng},
  number       = {2},
  pages        = {173--185},
  title        = {Building trophic specializations that result in substantial niche partitioning within a young adaptive radiation},
  url          = {http://dx.doi.org/10.1111/joa.12742},
  volume       = {232},
  year         = {2018},
}

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