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Abstract Adaptive radiations are striking examples of rapid speciation along ecological lines. In adaptive radiations, fast rates of lineage diversification often pair with rapid rates of morphological diversification. Such diversification has often been documented through the lens of ecological drivers, overlooking the intrinsic structural constraints that may also have a key role in configuring patterns of trait diversification. Covariation within and between traits has been hypothesized to govern the axes of trait evolution, either by increasing the degree of covariation between traits (i.e. integration), which promotes morphological coordination, or by strengthening the degree of covariation within traits (i.e. modularity), which allows organisms to explore novel trait combinations and different regions of morphospace. Here, we study the modularity of the skull within an adaptive radiation of pupfishes that is endemic to San Salvador Island, Bahamas. This radiation exhibits divergent craniofacial morphologies, including generalist, snail-eating specialist, and scale-eating specialist species. We assessed morphological disparity, integration strength, and modularity patterns across the sympatric San Salvador Island pupfish radiation, lab-reared hybrids, and closely related outgroup species. Our findings revealed an unexpected uniformity in the pattern of modularity across diverse species, supporting a five-module functional hypothesis comprising the oral jaw, pharyngeal jaw, neurocranium, hyoid apparatus, and hyomandibula. Despite this conserved modularity pattern, all species exhibited weak but significantly varying strengths of overall between-module integration and significant disparity across all cranial regions. Our results suggest rapid morphological diversification can occur even with conserved patterns of modularity. We propose that broadscale patterns of modularity are more conserved while between-module associations are more evolvable between species.
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Developmental and Functional Interactions Structure Patterns of Variational Modularity in the Lunar Wrasse Skull
Synopsis Trait modularity is a defining feature of complex life. However, the drivers of modularity across different scales of biological organization remain opaque. Studies have shown that a combination of developmental and functional interactions can structure patterns of trait covariation at the developmental, population, and even macroevolutionary level. However, it remains unclear how developmental and functional interactions may translate or influence macroevolutionary patterns of trait covariance and diversification. Pharyngognathy is a striking evolutionary innovation that has evolved multiple times in acanthomorph fishes and has resulted in the evolution of robust pharyngeal jaws that are used to process hard prey. Recent studies have found strong patterns of evolutionary integration among the jaw systems in pharyngognathous fishes suggesting that this innovation was brought about by the evolutionary coupling of two otherwise distinct trait complexes. Furthermore, the pharyngeal jaws have been hypothesized to act as a constraining force on the evolution of the oral jaws potentially due to their developmental origins in the more conserved hox-positive region of the skull. While multiple studies have recovered strong evolutionary integration between the jaw systems, patterns of modularity at the population (variational) level appear to differ, where a high degree of modularity has been found between the oral and pharyngeal jaws suggesting a disconnect between patterns of evolutionary modularity and patterns of variational modularity. Here, we are using three-dimensional geometric morphometrics to test for modularity between the oral and pharyngeal jaws at the variational level in a population of Lunar wrasse collected from Kagoshima, Japan and additionally test for differences in morphological disparity between the oral and pharyngeal jaws. We find strong support for a developmental hypothesis of modularity that separates the jaw systems into distinct modules. We additionally find mixed support for the constraint hypothesis of the pharyngeal jaws, where some elements of the pharyngeal jaws were found to exhibit less morphological disparity than the oral jaws while others exhibited more morphological disparity. Our findings suggest that developmental and functional interactions at the variational level may impart patterns of covariation that are distinct from evolutionary patterns of modularity that are found between species.
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- Award ID(s):
- 2237278
- PAR ID:
- 10680525
- Publisher / Repository:
- Integrative and Comparative Biology
- Date Published:
- Journal Name:
- Integrative And Comparative Biology
- Volume:
- 65
- Issue:
- 3
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 560 to 571
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/icb/icaf099
