skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Evolutionary innovation accelerates morphological diversification in pufferfishes and their relatives
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
Award ID(s):
2237278 2401223
PAR ID:
10552480
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Evolution
Volume:
78
Issue:
11
ISSN:
0014-3820
Format(s):
Medium: X Size: p. 1869-1882
Size(s):
p. 1869-1882
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    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
  2. 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
  3. Adaptive radiations are characterized by an increase in species and/or phenotypic diversity as organisms fill open ecological niches. Often, the putative adaptive radiation has been studied without explicit comparison to the patterns and rates of evolution of closely related clades, leaving open the question whether notable changes in evolutionary process indeed occurred at the origin of the group. Anolis lizards are an oft-used model for investigating the tempo and mode of adaptive radiations. Most of the prior research on the diversification of Anolis morphology has focused on the post-cranium because of its significance towards subdivision of the arboreal habitat. But the remarkable diversity in head shape in anoles has not been as thoroughly investigated. It remains unknown whether the tempo or mode of head shape diversification changed as anoles diversified. We performed geometric morphometric analysis of skull shape across a sample of 12 Iguanian families (110 species), including anoles. Anolis lizards occupy a unique area and a wider region of morphological space compared to the 11 other families examined. We did not find a difference in the evolutionary rate of head shape diversification between anoles and their relatives. Rather, the extraordinary amount of skull diversity arose through a distinct mode of evolution; anoles moved into novel regions by relatively large morphological transitions across morphological space compared to their relatives. Our results demonstrate that traits not directly tied to the adaptive shift of a lineage into unique ecological spaces may undergo exceptional patterns of change as the clade diversifies. 
    more » « less
  4. ABSTRACT Understanding how the intrinsic ability of populations and species to meet shifting selective demands shapes evolutionary patterns over both short and long timescales is a major question in biology. One major axis of evolutionary flexibility can be measured by phenotypic integration and modularity. The strength, scale, and structure of integration may constrain or catalyze evolution in the face of new selective pressures. We analyze a dataset of seven leaf measurements across Vitaceae to examine how correlations in trait divergence are linked to transitions between freezing and nonfreezing habitats. We assess this by applying a custom algorithm to compare the timing of habitat shifts to changes in the structure of evolutionary trait correlation at discrete points along a phylogeny. We also explore these patterns in relation to lineage diversification rates to understand how and whether patterns in the evolvability of complex multivariate phenotypes are linked to higher‐level macroevolutionary dynamics. We found that shifts in the structure, but not the overall strength, of phylogenetic integration of leaves precipitate colonization of freezing climates. Lineages that underwent associated shifts in leaf trait integration and subsequent movement into freezing habitats also displayed lower turnover and higher net diversification, suggesting a link among shifting vectors of selection, internal constraint, and lineage persistence in the face of changing environments. 
    more » « less
  5. 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