The genomic architecture of convergent snail crushing jaws in cichlid fishes

• Applicant: Professor Dr. C. Darrin Hulsey
• Subject Area: Evolution, Anthropology
• Term: from 2017 to 2021
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 366312182

• Final Report Year: 2022

Final Report Abstract

Evolution can repeat itself. When phenotypes do evolve repeatedly in response to similar ecological conditions, we begin to have the power to test whether there are generalizable patterns to how selection and genomics work in concert to shape organismal adaptations. These convergent phenotypes provide strong evidence that there might be only a limited number of ways for the genome to produce the same phenotypes to solve similar ecological problems. For instance, very conspicuously convergent phenotypes that allow crushing hard-shelled prey have arisen during the repeated adaptive radiations of cichlid fishes. Until recently, it has been largely unknown what the underlying genomic architectures of these parallel radiations are. However, during the last few years, genomic tools have increasingly provided the ability to begin dissecting the genetic basis of phenotypes that have originated repeatedly. Crushing trophic phenotypes in cichlid fishes offer an ideal model system to address these types of analyses on repeated ecological adaptations and convergence. The main goal of this project was to increase knowledge of the molecular basis that underlies the repeated evolution of a characteristic cichlid trophic adaptation. Specifically, the aim of the proposed research program was to explore 1) the mechanistic basis of the dental polymorphism H. minckleyi and 2) the loci responsible for tooth and other trophic phenotypes in multiple cichlid groups. This project made important contributions to a better understanding of the mechanisms that underlie crushing adaptations in cichlid fishes, including: 1) Demonstrated that similar relationships exist between tooth numbers on the two jaws in both African Lake Victoria cichlids and across the phylogenetic diversity of Lake Malawi cichlids. This work suggested tooth numbers on the two jaws of haplochromine cichlids might generally coevolve owing to shared genetic underpinnings. 2) Established that several evolutionarily novel genes as well as genes known to be involved in fish tooth development form a gene cluster and underlie convergent evolution of enlarged teeth in cichlids. While the ecological benefit of evolving molar-like teeth to crush prey has been known, it was whether the same molecular mechanisms underlie these convergent traits. 3) Examined the genomic basis of allopatric and sympatric species divergence in the pharyngeal jaws and other adaptively diverging traits of Nicaraguan Midas cichlids. We found counter to conventional wisdom, that traits with simple genomic architectures were not the basis of sympatric divergence, but instead quantitative traits with multiple genetic changes were the basis if sympatric speciation. 4) Discussed the underlying physiological, developmental, and genetic mechanisms that generate phenotypic plasticity in teeth and attempted to clarify the role of plasticity in the evolution of dental phenotypes. 5) Found that cichlid fish sppecies with larger numbers of erupted pharyngeal teeth also had larger numbers of replacement teeth. Replacement tooth size is almost exactly predicted from the size of erupted teeth across numerous cichlid species suggesting there are general rules to how crushing dentitions are replaced. 6) Increased our understanding of how teeth serve as a model system for integrating developmental genomics, functional morphology, and evolution. This project generated an exceptional amount of molecular and phenotypic data. These extremely useful resources will foster further investigations on this exciting biological system.

Publications

• The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis chilotes x H. nyererei). G3 Genes|Genomes|Genetics, 7(9), 3195-3202.
  Hulsey, C Darrin; Machado-Schiaffino, Gonzalo; Keicher, Lara; Ellis-Soto, Diego; Henning, Frederico & Meyer, Axel
  
• A Genomic Cluster Containing Novel and Conserved Genes is Associated with Cichlid Fish Dental Developmental Convergence. Molecular Biology and Evolution, 37(11), 3165-3174.
  Karagic, Nidal; Schneider, Ralf F; Meyer, Axel & Hulsey, C Darrin
  
• Contrasting signatures of genomic divergence during sympatric speciation. Nature, 588(7836), 106-111.
  Kautt, Andreas F.; Kratochwil, Claudius F.; Nater, Alexander; Machado-Schiaffino, Gonzalo; Olave, Melisa; Henning, Frederico; Torres-Dowdall, Julián; Härer, Andreas; Hulsey, C. Darrin; Franchini, Paolo; Pippel, Martin; Myers, Eugene W. & Meyer, Axel
  
• Convergent Evolution of Cichlid Fish Pharyngeal Jaw Dentitions in Mollusk-Crushing Predators: Comparative X-Ray Computed Tomography of Tooth Sizes, Numbers, and Replacement. Integrative and Comparative Biology, 60(3), 656-664.
  Hulsey, C Darrin; Meyer, Axel & Streelman, J Todd
  
• Grand Challenges in Comparative Tooth Biology. Integrative and Comparative Biology, 60(3), 563-580.
  Hulsey, C. Darrin; Cohen, Karly E.; Johanson, Zerina; Karagic, Nidal; Meyer, Axel; Miller, Craig T.; Sadier, Alexa; Summers, Adam P. & Fraser, Gareth J.
  
• Phenotypic Plasticity in Vertebrate Dentitions. Integrative and Comparative Biology, 60(3), 608-618.
  Karagic, Nidal; Meyer, Axel & Hulsey, C Darrin