Dietary adaptations — that is, all adaptations related to how nutrients are acquired and processed — play a central role in the evolution and maintenance of organismal diversity on Earth in general and in adaptive radiations of species in particular. In vertebrates, the trophic process can be divided into two fundamental components: food uptake and digestion. Through a timely combination of state-of-the-art genomics technologies and broad phylogenetic sampling, it is now possible to elucidate the molecular and developmental underpinnings of both feeding-related structures (e.g., jaws or teeth) and the digestive system at unprecedented resolution, as well as to evaluate their contributions to adaptation and diversification.
In the framework of this Sinergia proposal, we put forward an interdisciplinary and integrative approach, focusing our efforts towards a comprehensive understanding of dietary adaptations in the digestive system. Our multi-faceted approach is only possible through the joint expertise, research infrastructure, methodological skill-set, and biological samples of the consortium labs, thereby allowing each lab to expand substantially beyond their previous lines of research. Specifically, we propose a systematic and large-scale survey of dietary adaptations and their underlying morphological, cellular and gene regulatory changes across feeding strategies, key digestive organs (intestine and liver) and developmental stages in two prominent evolutionary radiations in vertebrates — of cichlid fishes from Lake Tanganyika and eutherian mammals — that cover both short (<6-9 million years, cichlids) and long (=75 million years, mammals) evolutionary time scales.
Our work plan is guided by a number of specific hypotheses. First, we hypothesize that digestive organ adaptations typically arise late in development, facilitated by decreased selective constraints. Second, while all major mutational types likely contributed to dietary adaptations in both cichlids and mammals, we conjecture that the predominant mutational mechanism is cis-regulatory changes in old genes in cichlids, as the short radiation time in this clade likely limited the accumulation of less rapidly accumulating coding mutations. Third, we predict that dietary novelties involved evolutionary changes in gene expression programs and the cellular composition of the digestive organs, and that all mutational types contributed to cell compositional changes. However, we surmise that new gene origination was key for the emergence of novel cell types, and that new cell types played a more prominent role for intestine than liver adaptations. Fourth, we hypothesize that the mechanisms and degree of phenotypic plasticity, leading to differences in intestine/liver anatomy and function, vary across development (i.e., more plasticity later in development) and between the two radiations (i.e., higher morphological plasticity in cichlids, but similar contributions of gene expression changes to phenotypic plasticity in cichlids and mammals). Finally, we note that our analyses of the unique and novel datasets generated in the proposed project will allow us to assess various general questions in an exploratory fashion, which will result in novel hypotheses to be tested in the future.
Our current predictions, research questions, and anticipated novel hypotheses, will be evaluated in the framework of four complementary goals. First, we will scrutinize the morphological features of the digestive system across development of representative cichlids using computed tomography scans and histological methods, which will set the stage for all subsequent molecular/cellular comparisons among cichlids and between cichlids and mammals. Second, we will generate and analyze extensive bulk and single-cell transcriptome data for the intestine and liver across development and adult stages of representative cichlids and mammals. We will thus trace evolutionary changes of gene expression programs and cellular compositions that underlie digestive organ innovations. Third, we will generate matched single-cell epigenomic datasets to explore the gene regulatory foundations of digestive organ development and adaptation. Finally, we will carry out dedicated feeding experiments in selected cichlids and a mammal (rat) to assess the extent to which adaptations may rapidly occur through phenotypic plasticity (i.e., developmental plasticity at the morphological, cellular, and molecular levels) rather than "hard-wired" genetic changes in the two vertebrate groups, respectively.
By contextualizing our anticipated results within the frameworks of dietary ecology and comparative digestive physiology, our work will substantially advance our understanding of the molecular, cellular and morphological evolution of dietary adaptations across different timescales and thus provide a novel and unique perspective on the evolution of vertebrates, including our own species.
