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: Evolution of vertebrate gill covers via shifts in an ancient Pou3f3 enhancer
Significance The evolution of jaws in early vertebrates provided such a predatory advantage that 99% of vertebrate species living today are jawed. What is often overlooked, however, is another structural innovation that happened concurrently and may have been equally critical to the lineage’s success: the evolution of musculoskeletal gill covers to actively drive oxygenated water over the gills. Here, we identify the first essential gene for gill cover formation in modern vertebrates, Pou3f3, and uncover the genomic element that brought Pou3f3 expression into the pharynx more than 430 Mya. Remarkably, small changes in this deeply conserved sequence account for the single large gill cover in living bony fish versus the five separate covers of sharks and their brethren.  more » « less
Award ID(s):
1656843
PAR ID:
10193145
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
117
Issue:
40
ISSN:
0027-8424
Format(s):
Medium: X Size: p. 24876-24884
Size(s):
p. 24876-24884
Sponsoring Org:
National Science Foundation
More Like this
  1. Jawed vertebrates (gnathostomes) have been the dominant lineage of deuterostomes for nearly three hundred fifty million years. Only a few lineages of jawless vertebrates remain in comparison. Composed of lampreys and hagfishes (cyclostomes), these jawless survivors are important systems for understanding the evolution of vertebrates. One focus of cyclostome research has been head skeleton development, as its evolution has been a driver of vertebrate morphological diversification. Recent work has identified hyaline-like cartilage in the oral cirri of the invertebrate chordate amphioxus, making cyclostomes critical for understanding the stepwise acquisition of vertebrate chondroid tissues. Our knowledge of cyclostome skeletogenesis, however, has lagged behind gnathostomes due to the difficulty of manipulating lamprey and hagfish embryos. In this review, we discuss and compare the regulation and histogenesis of cyclostome and gnathostome skeletal tissues. We also survey differences in skeletal morphology that we see amongst cyclostomes, as few elements can be confidently homologized between them. A recurring theme is the heterogeneity of skeletal morphology amongst living vertebrates, despite conserved genetic regulation. Based on these comparisons, we suggest a model through which these mesenchymal connective tissues acquired distinct histologies and that histological flexibility in cartilage existed in the last common ancestor of modern vertebrates. 
    more » « less
  2. Abstract Species introductions provide opportunities to quantify rates and patterns of evolutionary change in response to novel environments. Alewives (Alosa pseudoharengus) are native to the East Coast of North America where they ascend coastal rivers to spawn in lakes and then return to the ocean. Some populations have become landlocked within the last 350 years and diverged phenotypically from their ancestral marine population. More recently, alewives were introduced to the Laurentian Great Lakes (~150 years ago), but these populations have not been compared to East Coast anadromous and landlocked populations. We quantified 95 years of evolution in foraging traits and overall body shape of Great Lakes alewives and compared patterns of phenotypic evolution of Great Lakes alewives to East Coast anadromous and landlocked populations. Our results suggest that gill raker spacing in Great Lakes alewives has evolved in a dynamic pattern that is consistent with responses to strong but intermittent eco‐evolutionary feedbacks with zooplankton size. Following their initial colonization of Lakes Ontario and Michigan, dense alewife populations likely depleted large‐bodied zooplankton, which drove a decrease in alewife gill raker spacing. However, the introduction of large, non‐native zooplankton to the Great Lakes in later decades resulted in an increase in gill raker spacing, and present‐day Great Lakes alewives have gill raker spacing patterns that are similar to the ancestral East Coast anadromous population. Conversely, contemporary Great Lakes alewife populations possess a gape width consistent with East Coast landlocked populations. Body shape showed remarkable parallel evolution with East Coast landlocked populations, likely due to a shared response to the loss of long‐distance movement or migrations. Our results suggest the colonization of a new environment and cessation of migration can result in rapid parallel evolution in some traits, but contingency also plays a role, and a dynamic ecosystem can also yield novel trait combinations. 
    more » « less
  3. Vertebrate vision is accomplished through light-sensitive photopigments consisting of an opsin protein bound to a chromophore. In dim light, vertebrates generally rely on a single rod opsin [rhodopsin 1 (RH1)] for obtaining visual information. By inspecting 101 fish genomes, we found that three deep-sea teleost lineages have independently expanded their RH1 gene repertoires. Among these, the silver spinyfin (Diretmus argenteus) stands out as having the highest number of visual opsins in vertebrates (two cone opsins and 38 rod opsins). Spinyfins express up to 14 RH1s (including the most blueshifted rod photopigments known), which cover the range of the residual daylight as well as the bioluminescence spectrum present in the deep sea. Our findings present molecular and functional evidence for the recurrent evolution of multiple rod opsin–based vision in vertebrates. 
    more » « less
  4. Abstract Suction feeding and gill ventilation in teleosts are functionally coupled, meaning that there is an overlap in the structures involved with both functions. Functional coupling is one type of morphological integration, a term that broadly refers to any covariation, correlation, or coordination among structures. Suction feeding and gill ventilation exhibit other types of morphological integration, including functional coordination (a tendency of structures to work together to perform a function) and evolutionary integration (a tendency of structures to covary in size or shape across evolutionary history). Functional coupling, functional coordination, and evolutionary integration have each been proposed to limit morphological diversification to some extent. Yet teleosts show extraordinary cranial diversity, suggesting that there are mechanisms within some teleost clades that promote morphological diversification, even within the highly integrated suction feeding and gill ventilatory systems. To investigate this, we quantified evolutionary integration among four mechanical units associated with suction feeding and gill ventilation in a diverse clade of benthic, primarily suction-feeding fishes (Cottoidei; sculpins and relatives). We reconstructed cottoid phylogeny using molecular data from 108 species, and obtained 24 linear measurements of four mechanical units (jaws, hyoid, opercular bones, and branchiostegal rays) from micro-CT reconstructions of 44 cottoids and 1 outgroup taxon. We tested for evolutionary correlation and covariation among the four mechanical units using phylogenetically corrected principal component analysis to reduce the dimensionality of measurements for each unit, followed by correlating phylogenetically independent contrasts and computing phylogenetic generalized least squares models from the first principle component axis of each of the four mechanical units. The jaws, opercular bones, and branchiostegal rays show evolutionary integration, but the hyoid is not positively integrated with these units. To examine these results in an ecomorphological context, we used published ecological data in phylogenetic ANOVA models to demonstrate that the jaw is larger in fishes that eat elusive or grasping prey (e.g., prey that can easily escape or cling to the substrate) and that the hyoid is smaller in intertidal and hypoxia-tolerant sculpins. Within Cottoidei, the relatively independent evolution of the hyoid likely has reduced limitations on morphological evolution within the highly morphologically integrated suction feeding and gill ventilatory systems. 
    more » « less
  5. Abstract Fish are the most diverse and widely distributed vertebrates, yet little is known about the microbial ecology of fishes nor the biological and environmental factors that influence fish microbiota. To identify factors that explain microbial diversity patterns in a geographical subset of marine fish, we analyzed the microbiota (gill tissue, skin mucus, midgut digesta and hindgut digesta) from 101 species of Southern California marine fishes, spanning 22 orders, 55 families and 83 genera, representing ~25% of local marine fish diversity. We compare alpha, beta and gamma diversity while establishing a method to estimate microbial biomass associated with these host surfaces. We show that body site is the strongest driver of microbial diversity while microbial biomass and diversity is lowest in the gill of larger, pelagic fishes. Patterns of phylosymbiosis are observed across the gill, skin and hindgut. In a quantitative synthesis of vertebrate hindguts (569 species), we also show that mammals have the highest gamma diversity when controlling for host species number while fishes have the highest percent of unique microbial taxa. The composite dataset will be useful to vertebrate microbiota researchers and fish biologists interested in microbial ecology, with applications in aquaculture and fisheries management. 
    more » « less