Lower Pharyngeal Jaw Shape Research Articles

Tracing evolutionary decoupling of oral and pharyngeal jaws in cichlid fishes.

Evolutionary innovations can facilitate diversification if the novel trait enables a lineage to exploit new niches or by expanding character space. The elaborate pharyngeal jaw apparatus of cichlid fishes is often referred to as an evolutionary “key innovation” that has promoted the spectacular adaptive radiations in these fishes. This goes back to the idea that the structural and functional independence of the oral and pharyngeal jaws for food capturing and food processing, respectively, permitted each jaw type to follow independent evolutionary trajectories. This “evolutionary decoupling” is thought to have facilitated novel trait combinations and, hence, ecological specialization, ultimately allowing more species to coexist in sympatry. Here, we test the hypotheses of evolutionary decoupling of the oral and pharyngeal jaws in the massive adaptive radiation of cichlid fishes in African Lake Tanganyika. Based on phylogenetic comparative analyses of oral jaw morphology and lower pharyngeal jaw shape across most of the ∼240 cichlid species occurring in that lake, we show that the two jaws evolved coupled along the main axes of morphological variation, yet most other components of these trait complexes evolved largely independently over the course of the radiation. Further, we find limited correlations between the two jaws in both overall divergence and evolutionary rates. Moreover, we show that the two jaws were evolutionary decoupled at a late stage of the radiation, suggesting that decoupling contributed to micro‐niche partitioning and the associated rapidly increasing trophic diversity during this phase.

Drivers and dynamics of a massive adaptive radiation in cichlid fishes.

Adaptive radiation is the likely source of much of the ecological and morphological diversity of life1-4. How adaptive radiations proceed and what determines their extent remains unclear in most cases1,4. Here we report the in-depth examination of the spectacular adaptive radiation of cichlid fishes in Lake Tanganyika. On the basis of whole-genome phylogenetic analyses, multivariate morphological measurements of three ecologically relevant trait complexes (body shape, upper oral jaw morphology and lower pharyngeal jaw shape), scoring of pigmentation patterns and approximations of the ecology of nearly all of theapproximately 240 cichlid species endemic to Lake Tanganyika, we show that the radiation occurred within the confines of the lake and that morphological diversification proceeded in consecutive trait-specific pulses of rapid morphospace expansion. We provide empirical support for two theoretical predictions of how adaptive radiations proceed, the 'early-burst' scenario1,5 (for body shape) and the stages model1,6,7 (for all traits investigated). Through the analysis of two genomes per species and by taking advantage of the uneven distribution of species in subclades of the radiation, we further show that species richness scales positively with per-individual heterozygosity, but is not correlated with transposable element content, number of gene duplications or genome-wide levels of selection in coding sequences.

Feeding ecomorphologies in the fish genus Herichthys (Perciformes: Cichlidae) based on stomach content and lower pharyngeal jaw shape

Speciation is a multifactorial process with factors acting at different scales of space and time. Trophic niche segregation has promoted the diversification of cichlids fishes in lentic (lacustrine) environments, whether this is also the case in lotic (riverine) systems remains unknown. Herichthys is the genus of cichlids with the most boreal distribution in the Americas comprising 12 currently recognized species, most micro-endemic and only two with a wide distribution. In the present work, we analyzed the stomach content and lower pharyngeal jaw morphologies of the species of the genus to evaluate the possible role of feeding ecology in the diversification of the group. Trophic strategies varied widely, including omnivores, piscivores, invertivores, molluskivores, detritivores, herbivores and algivores. Low values of Pianka's index of niche overlap were found in the sympatric micro-endemic species, while in the widely distributed species the indices ranged from low to very high. The analysis of lower pharyngeal jaw morphologies allowed discriminating a shape associated with piscivorous species from other foraging groups. The results of this study suggest that trophic niche segregation is a factor that could promotes diversification within the genus Herichthys although additional studies need to be performed to fully understand the speciation process in this group of Neotropical cichlid fishes.

Ecological diversification associated with the pharyngeal jaw diversity of Neotropical cichlid fishes.

Innovations can facilitate bursts of diversification by increasing access to novel resources and the attainment of novel functional designs. Pharyngognathy, exhibited by highly diverse groups such as wrasses and cichlid fishes, is hypothesized to increase foraging capacity and efficiency. Here, I test the hypothesis that pharyngeal jaw shape and tooth morphology are adaptive in an ecologically diverse radiation of Neotropical cichlid fishes that spans North, Central and South America. I partitioned species into generalized trophic guilds using published stomach content analyses and quantified shape variation of the lower pharyngeal jaw (LPJ) using geometric morphometrics. Additionally, I tested for convergence in LPJ shape and trophic guild by mapping the phylogeny onto the principal components and testing for shifts towards similar evolutionary regimes. Major LPJ shape variation included the length and orientation (i.e. narrow or wide) of the lateral processes and length of the medial process, which varied based on the proportion of fishes and plants consumed. Pharyngeal tooth number, diversity and the frequency of tooth types were not evenly distributed among trophic guilds. There were seven distinct evolutionary regimes that converged upon four optima. Pharyngeal jaw diversification is associated with the exploitation of novel resources among Neotropical cichlids such that pharyngeal specialization has increased access to otherwise poorly accessible resources, such as resources that are difficult to crush (e.g. hard-shelled organisms) and assimilate (e.g. algae).

Rates of piscivory predict pharyngeal jaw morphology in a piscivorous lineage of cichlid fishes

AbstractThe pharyngeal jaw apparatus is a key innovation hypothesised to increase foraging efficiency and facilitate utilisation of novel resources among teleost fishes. Here, we tested whether dietary characteristics could predict pharyngeal jaw morphology among eight species of Neotropical Crenicichla. Additionally, we tested the hypothesis that pharyngeal jaws may impose a functional constraint on piscivory via pharyngeal gape. We quantified the shape of the lower pharyngeal jaw (LPJ) using linear and geometric morphometrics and quantified diet using the relative volumetric proportions of prey items. We used principal component analysis to describe major axes of variation in LPJ shape and dietary patterns. The major axis of dietary variation significantly predicted LPJ morphology, which was driven by a significant relationship between LPJ shape and rates of piscivory. We also found that rates of piscivory predicted size‐corrected LPJ depth. Size‐corrected pharyngeal gape also significantly predicted rates of piscivory such that pharyngeal jaws may constrain piscivory by limiting pharyngeal gape. Strong form‐to‐function linkage between pharyngeal morphology and trophic patterns suggests an adaptive quality of the pharyngeal apparatus but may also impose functional constraints when consumers must switch prey or when prey availability is temporally or spatially unpredictable.

Allometric shape change of the lower pharyngeal jaw correlates with a dietary shift to piscivory in a cichlid fish

The morphological versatility of the pharyngeal jaw of cichlid fishes is assumed to represent a key factor facilitating their unparalleled trophic diversification and explosive radiation. It is generally believed that the functional design of an organism relates to its ecology, and thus, specializations to different diets are typically associated with distinct morphological designs, especially manifested in the cichlids' pharyngeal jaw apparatus. Thereby, the lower pharyngeal jaw (LPJ) incorporates some of the most predictive features for distinct diet-related morphotypes. Thus, considering that piscivorous cichlids experience an ontogenetic dietary shift from typically various kinds of invertebrates to fish, concomitant morphological changes in the LPJ are expected. Using Lepidiolamprologus elongatus, a top predator in the shallow rocky habitat of Lake Tanganyika, as model, and applying geometric and traditional morphometric techniques, we demonstrate an allometric change in ontogenetic LPJ shape development coinciding with the completion of the dietary shift toward piscivory. The piscivorous LPJ morphotype is initiated in juvenile fish by increasing elongation and narrowing of the LPJ and--when the fish reach a size of 80-90 mm standard length--further refined by the elongation of the posterior muscular processes, which serve as insertion for the fourth musculus levator externus. The enlarged muscular processes of the fully mature piscivorous morphotype provide for the construction of a powerful lever system, which allows the large individuals to process large prey fish and rely on exclusive piscivory.