Linking conceptual mechanisms and transcriptomic evidence of plasticity-driven diversification (original) (raw)
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Adaptive phenotypic plasticity, the ability of an organism to change its phenotype to match local environments, is increasingly recognized for its contribution to evolution. However, few empirical studies have explored the molecular basis of plastic traits. The East African cichlid fish Astatoreochromis alluaudi displays adaptive phenotypic plasticity in its pharyngeal jaw apparatus, a structure that is widely seen as an evolutionary key innovation that has contributed to the remarkable diversity of cichlid fishes. It has previously been shown that in response to different diets, the pharyngeal jaws change their size, shape and dentition: hard diets induce an adaptive robust molariform tooth phenotype with short jaws and strong internal bone structures, while soft diets induce a gracile papilliform tooth phenotype with elongated jaws and slender internal bone structures. To gain insight into the molecular underpinnings of these adaptations and enable future investigations of the role that phenotypic plasticity plays during the formation of adaptive radiations, the transcriptomes of the two divergent jaw phenotypes were examined. Our study identified a total of 187 genes whose expression differs in response to hard and soft diets, including immediate early genes, extracellular matrix genes and inflammatory factors. Transcriptome results are interpreted in light of expression of candidate genes-markers for tooth size and shape, bone cells and mechanically sensitive pathways. This study opens up new avenues of research at new levels of biological organization into the roles of phenotypic plasticity during speciation and radiation of cichlid fishes.
BMC Evolutionary Biology, 2019
Background: Understanding how variation in gene expression contributes to morphological diversity is a major goal in evolutionary biology. Cichlid fishes from the East African Great lakes exhibit striking diversity in trophic adaptations predicated on the functional modularity of their two sets of jaws (oral and pharyngeal). However, the transcriptional basis of this modularity is not so well understood, as no studies thus far have directly compared the expression of genes in the oral and pharyngeal jaws. Nor is it well understood how gene expression may have contributed to the parallel evolution of trophic morphologies across the replicate cichlid adaptive radiations in Lake Tanganyika, Malawi and Victoria.
Gene coexpression networks reveal molecular interactions underlying cichlid jaw modularity
BMC Ecology and Evolution
BackgroundThe oral and pharyngeal jaw of cichlid fishes are a classic example of evolutionary modularity as their functional decoupling boosted trophic diversification and contributed to the success of cichlid adaptive radiations. Most studies until now have focused on the functional, morphological, or genetic aspects of cichlid jaw modularity. Here we extend this concept to include transcriptional modularity by sequencing whole transcriptomes of the two jaws and comparing their gene coexpression networks.ResultsWe show that transcriptional decoupling of gene expression underlies the functional decoupling of cichlid oral and pharyngeal jaw apparatus and the two units are evolving independently in recently diverged cichlid species from Lake Tanganyika. Oral and pharyngeal jaw coexpression networks reflect the common origin of the jaw regulatory program as there is high preservation of gene coexpression modules between the two sets of jaws. However, there is substantial rewiring of ge...
Baby fish working out: an epigenetic source of adaptive variation in the cichlid jaw
Proceedings of the Royal Society B: Biological Sciences, 2017
Understanding the developmental processes that underlie the production of adaptive variation (i.e. the ‘arrival of the fittest’) is a major goal of evolutionary biology. While most evo-devo studies focus on the genetic underpinnings of adaptive phenotypic variation, factors beyond changes in nucleotide sequence can also play a major role in shaping developmental outcomes. Here, we document a vigorous but enigmatic gaping behaviour during the early development of Lake Malawi cichlid larvae. The onset of the behaviour precedes the formation of bone, and we predicted that it might influence craniofacial shape by affecting the mechanical environment in which bone develops. Consistent with this, we found that both natural variation and experimental manipulation of this behaviour induced differential skeletal development that foreshadows adaptive variation in adult trophic morphology. In fact, the magnitude of difference in skeletal morphology induced by these simple shifts in behaviour w...
Molecular ecology, 2014
Many organisms can produce alternative phenotypes in direct response to different environmental conditions, a phenomenon known as phenotypic plasticity. The environmentally sensitive gene regulatory networks (GRNs) that mediate such developmental flexibility are largely unknown. Yet, characterizing these GRNs is important not only for elucidating plasticity's molecular basis, but also for shedding light onto whether and how plasticity might impact evolution. In this issue of Molecular Ecology, Schneider et al.) describe one of the first efforts to determine the GRN underlying a plastic trait. They focus on diet-induced plasticity in the cichlid fish, Astatoreochromis alluaudi. Depending on whether soft food (e.g. insects) or hard food (e.g. molluscs) is consumed, this species forms a lower pharyngeal jaw (LPJ) with many fine teeth or with fewer molar-like teeth, respectively (Fig. 1). The authors previously identified genes that are differentially expressed between LPJ morphs du...
Molecular Biology and Evolution, 2020
The two toothed jaws of cichlid fishes provide textbook examples of convergent evolution. Tooth phenotypes such as enlarged molar-like teeth used to process hard-shelled mollusks have evolved numerous times independently during cichlid diversification. Although the ecological benefit of molar-like teeth to crush prey is known, it is unclear whether the same molecular mechanisms underlie these convergent traits. To identify genes involved in the evolution and development of enlarged cichlid teeth, we performed RNA-seq on the serially homologous-toothed oral and pharyngeal jaws as well as the fourth toothless gill arch of Astatoreochromis alluaudi. We identified 27 genes that are highly upregulated on both tooth-bearing jaws compared with the toothless gill arch. Most of these genes have never been reported to play a role in tooth formation. Two of these genes (unk, rpfA) are not found in other vertebrate genomes but are present in all cichlid genomes. They also cluster genomically with two other highly expressed tooth genes (odam, scpp5) that exhibit conserved expression during vertebrate odontogenesis. Unk and rpfA were confirmed via in situ hybridization to be expressed in developing teeth of Astatotilapia burtoni. We then examined expression of the cluster's four genes in six evolutionarily independent and phylogenetically disparate cichlid species pairs each with a large-and a small-toothed species. Odam and unk commonly and scpp5 and rpfA always showed higher expression in larger toothed cichlid jaws. Convergent trophic adaptations across cichlid diversity are associated with the repeated developmental deployment of this genomic cluster containing conserved and novel cichlid-specific genes.
Biting into the Genome to Phenome Map: Developmental Genetic Modularity of Cichlid Fish Dentitions
Integrative and Comparative Biology, 2016
Synopsis Within vertebrates, teleost fishes provide a rich evolutionary context for studying the mechanisms of dental divergence because of the numerous axes along which their teeth have diverged phenotypically and presumably developmentally. Using both a review of teleost in situ hybridization and de novo transcriptome sequencing in a cichlid fish, we examined whether 341 gene homologs thought to play a role in developing mice teeth are expressed in the tooth-bearing jaws of teleosts. The similarities and putative differences in gene expression documented between the two most commonly used models, zebrafish and cichlids, highlight what can be learned from using a greater diversity of teleost model systems in studies of tooth development. Both types of gene expression analysis also provide substantial evidence for conservation of tooth gene expression from teleosts to mammals as well as between initial and replacement teeth. Additionally, we found that the cichlid oral and pharyngeal jaws share expression for a large percentage of genes that influence tooth development. Our transcriptome analyses also suggest sub-functionalization between gene paralogs expressed in teeth and paralogs expressed in other structures is likely a common pattern across teleost diversity. Teleost dentitions will continue to provide a potent system in which to examine the importance of both gene duplication as well as the conservation of gene expression for phenotypic diversification.
Craniofacial divergence and ongoing adaptation via the hedgehog pathway
Proceedings of the National Academy of Sciences of the United States of America, 2011
Adaptive variation in craniofacial structure contributes to resource specialization and speciation, but the genetic loci that underlie craniofacial adaptation remain unknown. Here we show that alleles of the hedgehog pathway receptor Patched1 (Ptch1) gene are responsible for adaptive variation in the shape of the lower jaw both within and among genera of Lake Malawi cichlid fish. The evolutionarily derived allele of Ptch1 reduces the length of the retroarticular (RA) process of the lower jaw, a change predicted to increase speed of jaw rotation for improved suction-feeding. The alternate allele is associated with a longer RA and a more robustly mineralized jaw, typical of species that use a biting mode of feeding. Genera with the most divergent feeding morphologies are nearly fixed for different Ptch1 alleles, whereas species with intermediate morphologies still segregate variation at Ptch1. Thus, the same alleles that help to define macroevolutionary divergence among genera also co...
BMC Evolutionary Biology, 2011
Background: Phenotypic evolution and its role in the diversification of organisms is a central topic in evolutionary biology. A neglected factor during the modern evolutionary synthesis, adaptive phenotypic plasticity, more recently attracted the attention of many evolutionary biologists and is now recognized as an important ingredient in both population persistence and diversification. The traits and directions in which an ancestral source population displays phenotypic plasticity might partly determine the trajectories in morphospace, which are accessible for an adaptive radiation, starting from the colonization of a novel environment. In the case of repeated colonizations of similar environments from the same source population this "flexible stem" hypothesis predicts similar phenotypes to arise in repeated subsequent radiations. The Midas Cichlid (Amphilophus spp.) in Nicaragua has radiated in parallel in several crater-lakes seeded by populations originating from the Nicaraguan Great Lakes. Here, we tested phenotypic plasticity in the pharyngeal jaw of Midas Cichlids. The pharyngeal jaw apparatus of cichlids, a second set of jaws functionally decoupled from the oral ones, is known to mediate ecological specialization and often differs strongly between sister-species. Results: We performed a common garden experiment raising three groups of Midas cichlids on food differing in hardness and calcium content. Analyzing the lower pharyngeal jaw-bones we find significant differences between diet groups qualitatively resembling the differences found between specialized species. Observed differences in pharyngeal jaw expression between groups were attributable to the diet's mechanical resistance, whereas surplus calcium in the diet was not found to be of importance.
Molecular ecology, 2012
The study of parallel evolution facilitates the discovery of common rules of diversification. Here, we examine the repeated evolution of thick lips in Midas cichlid fishes (the Amphilophus citrinellus species complex)-from two Great Lakes and two crater lakes in Nicaragua-to assess whether similar changes in ecology, phenotypic trophic traits and gene expression accompany parallel trait evolution. Using next-generation sequencing technology, we characterize transcriptome-wide differential gene expression in the lips of wild-caught sympatric thick-and thin-lipped cichlids from all four instances of repeated thick-lip evolution. Six genes (apolipoprotein D, myelin-associated glycoprotein precursor, four-and-a-half LIM domain protein 2, calpain-9, GTPase IMAP family member 8-like and one hypothetical protein) are significantly underexpressed in the thick-lipped morph across all four lakes. However, other aspects of lips' gene expression in sympatric morphs differ in a lake-specific pattern, including the magnitude of differentially expressed genes (97-510). Generally, fewer genes are differentially expressed among morphs in the younger crater lakes than in those from the older Great Lakes. Body shape, lower pharyngeal jaw size and shape, and stable isotopes (d 13 C and d 15 N) differ between all sympatric morphs, with the greatest differentiation in the Great Lake Nicaragua. Some ecological traits evolve in parallel (those related to foraging ecology; e.g. lip size, body and head shape) but others, somewhat surprisingly, do not (those related to diet and food processing; e.g. jaw size and shape, stable isotopes). Taken together, this case of parallelism among thick-and thin-lipped cichlids shows a mosaic pattern of parallel and nonparallel evolution.