Abstract Evolutionary innovations have played an important role in shaping the diversity of life on Earth. However, how these innovations arise and their downstream effects on patterns of morphological diversification remain poorly understood. Here, we examine the impact of evolutionary innovation on trait diversification in tetraodontiform fishes (pufferfishes, boxfishes, ocean sunfishes, and allies). This order provides an ideal model system for studying morphological diversification owing to their range of habitats and divergent morphologies, including the fusion of the teeth into a beak in several families. Using three-dimensional geometric morphometric data for 176 extant and fossil species, we examine the effect of skull integration and novel habitat association on the evolution of innovation. Strong integration may be a requirement for rapid trait evolution and facilitating the evolution of innovative structures, like the tetraodontiform beak. Our results show that the beak arose in the presence of highly conserved patterns of integration across the skull, suggesting that integration did not limit the range of available phenotypes to tetraodontiforms. Furthermore, we find that beaks have allowed tetraodontiforms to diversify into novel ecological niches, irrespective of habitat. Our results suggest that general rules pertaining to evolutionary innovation may be more nuanced than previously thought. 
                        more » 
                        « less   
                    
                            
                            Integration drives rapid phenotypic evolution in flatfishes
                        
                    
    
            Evolutionary innovations are scattered throughout the tree of life, and have allowed the organisms that possess them to occupy novel adaptive zones. While the impacts of these innovations are well documented, much less is known about how these innovations arise in the first place. Patterns of covariation among traits across macroevolutionary time can offer insights into the generation of innovation. However, to date, there is no consensus on the role that trait covariation plays in this process. The evolution of cranial asymmetry in flatfishes (Pleuronectiformes) from within Carangaria was a rapid evolutionary innovation that preceded the colonization of benthic aquatic habitats by this clade, and resulted in one of the most bizarre body plans observed among extant vertebrates. Here, we use three-dimensional geometric morphometrics and a phylogenetic comparative toolkit to reconstruct the evolution of skull shape in carangarians, and quantify patterns of integration and modularity across the skull. We find that the evolution of asymmetry in flatfishes was a rapid process, resulting in the colonization of novel trait space, that was aided by strong integration that coordinated shape changes across the skull. Our findings suggest that integration plays a major role in the evolution of innovation by synchronizing responses to selective pressures across the organism. 
        more » 
        « less   
        
    
                            - Award ID(s):
- 1852096
- PAR ID:
- 10230577
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 18
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- e2101330118
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
- 
            
- 
            Abstract Complex structures, like the vertebrate skull, are composed of numerous elements or traits that must develop and evolve in a coordinated manner to achieve multiple functions. The strength of association among phenotypic traits (i.e., integration), and their organization into highly-correlated, semi-independent subunits termed modules, is a result of the pleiotropic and genetic correlations that generate traits. As such, patterns of integration and modularity are thought to be key factors constraining or facilitating the evolution of phenotypic disparity by influencing the patterns of variation upon which selection can act. It is often hypothesized that selection can reshape patterns of integration, parceling single structures into multiple modules or merging ancestrally semi-independent traits into a strongly correlated unit. However, evolutionary shifts in patterns of trait integration are seldom assessed in a unified quantitative framework. Here, we quantify patterns of evolutionary integration among regions of the archosaur skull to investigate whether patterns of cranial integration are conserved or variable across this diverse group. Using high-dimensional geometric morphometric data from 3D surface scans and computed tomography scans of modern birds (n = 352), fossil non-avian dinosaurs (n = 27), and modern and fossil mesoeucrocodylians (n = 38), we demonstrate that some aspects of cranial integration are conserved across these taxonomic groups, despite their major differences in cranial form, function, and development. All three groups are highly modular and consistently exhibit high integration within the occipital region. However, there are also substantial divergences in correlation patterns. Birds uniquely exhibit high correlation between the pterygoid and quadrate, components of the cranial kinesis apparatus, whereas the non-avian dinosaur quadrate is more closely associated with the jugal and quadratojugal. Mesoeucrocodylians exhibit a slightly more integrated facial skeleton overall than the other grades. Overall, patterns of trait integration are shown to be stable among archosaurs, which is surprising given the cranial diversity exhibited by the clade. At the same time, evolutionary innovations such as cranial kinesis that reorganize the structure and function of complex traits can result in modifications of trait correlations and modularity.more » « less
- 
            Abstract Developmental and evolutionary processes underlying phenotypic variation frequently target several traits simultaneously, thereby causing covariation, or integration, among phenotypes. While phenotypic integration can be neutral, correlational selection can drive adaptive covariation. Especially, the evolution and development of exaggerated secondary sexual traits may require the adjustment of other traits that support, compensate for, or otherwise function in a concerted manner. Although phenotypic integration is ubiquitous, the interplay between genetic, developmental, and ecological conditions in shaping integration and its evolution remains poorly understood. Here, we study the evolution and plasticity of trait integration in the bull‐headed dung beetleOnthophagus tauruswhich is characterized by the polyphenic expression of horned (‘major’) and hornless (‘minor’) male morphs. By comparing populations subject to divergent intensities of mate competition, we tested whether mating system shifts affect integration of traits predicted to function in a morph‐specific manner. We focussed on fore and hind tibia morphology as these appendages are used to stabilize major males during fights, and on wings, as they are thought to contribute to morph‐based differences in dispersal behavior. We found phenotypic integration between fore and hind tibia length and horn length that was stronger in major males, suggesting phenotypic plasticity in integration and potentially secondary sexual trait compensation. Similarly, we observed that fore tibiashapewas also integrated with relative horn length. However, although we found population differentiation in wing and tibia shape and allometry, populations did not differ in integration. Lastly, we detected little evidence for morph differences in integration in either tibia or wing shape, although wing allometries differed between morphs. This contrasts with previous studies documenting intraspecific differentiation in morphology, behavior, and allometry as a response to varying levels of mate competition acrossO. tauruspopulations. We discuss how sexual selection may shape morph‐specific integration, compensation, and allometry across populations.more » « less
- 
            Abstract Integration is an essential feature of complex biomechanical systems, with coordination and covariation occurring among and within structural components at time scales that vary from microseconds to deep evolutionary time. Integration has been suggested to both promote and constrain morphological evolution, and the effects of integration on the evolution of structure likely vary by system, clade, historical contingency, and time scale. In this introduction to the 2019 symposium “Multifunctional Structures and Multistructural Functions,” we discuss the role of integration among structures in the context of functional integration and multifunctionality. We highlight articles from this issue of Integrative and Comparative Biology that explore integration within and among kinematics, sensory and motor systems, physiological systems, developmental processes, morphometric dimensions, and biomechanical functions. From these myriad examples it is clear that integration can exist at multiple levels of organization that can interact with adjacent levels to result in complex patterns of structural and functional phenotypes. We conclude with a synthesis of major themes and potential future directions, particularly with respect to using multifunctionality, itself, as a trait in evolutionary analyses.more » « less
- 
            Abstract An ongoing challenge in macroevolutionary research is identifying common drivers of diversification amid the complex interplay of many potentially relevant traits, ecological contexts, and intrinsic characteristics of clades. In this study, we used geometric morphometric and phylogenetic comparative methods to evaluate the tempo and mode of morphological evolution in an adaptive radiation of Malagasy birds, the vangas, and their mainland relatives (Aves:Vangidae). The Malagasy radiation is more diverse in both skull and foot shape. However, rather than following the classic “early burst” of diversification, trait evolution accelerated well after their arrival in Madagascar, likely driven by the evolution of new modes of foraging and especially of a few species with highly divergent morphologies. Anatomical regions showed differing evolutionary patterns, and the presence of morphological outliers impacted the results of some analyses, particularly of trait integration and modularity. Our results demonstrate that the adaptive radiation of Malagasy vangas has evolved exceptional ecomorphological diversity along multiple, independent trait axes, mainly driven by a late expansion in niche space due to key innovations. Our findings highlight the evolution of extreme forms as an overlooked feature of adaptive radiation warranting further study.more » « less
 An official website of the United States government
An official website of the United States government 
				
			 
					 
					
 
                                    