Developmental basis of phenotypic integration in two Lake Malawi cichlids.

Pierre Le Pabic,Thomas F. Schilling,W. James Cooper

doi:10.1186/s13227-016-0040-z

Pierre Le Pabic, Thomas F. Schilling + Show 1 more

Open Access

https://doi.org/10.1186/s13227-016-0040-z

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Abstract

BackgroundCichlid fishes from the Rift Lakes of East Africa have undergone the most spectacular adaptive radiations in vertebrate history. Eco-morphological adaptations in lakes Victoria, Malawi and Tanganyika have resulted in a vast array of skull shapes and sizes, yet primary axes of morphological variation are conserved in all three radiations, prominently including the size of the preorbital region of the skull. This conserved pattern suggests that development may constrain the trajectories of cichlid head morphological evolution.ResultsHere, we (1) present a comparative analysis of adult head morphology in two sand-dweller cichlids from Lake Malawi with preorbital size differences representative of the main axis of variation among the three lakes and (2) analyze the ontogeny of shape and size differences by focusing on known developmental modules throughout the head. We find that (1) developmental differences between the two species correlate with known developmental modules; (2) differences in embryonic cartilage development result in phenotypically integrated changes among all bones derived from a single cartilage, while differences in dermal bone development tend to influence isolated regions within a bone; and lastly (3) species-specific morphologies appear in the embryo as subtle differences, which become progressively amplified throughout ontogeny. We propose that this amplification takes place at skeletal growth zones, the locations and shapes of which are patterned during embryogenesis.ConclusionsThis study is the most anatomically comprehensive analysis of the developmental differences underlying cichlid skull evolution in the Rift Lakes of East Africa. The scale of our analysis reveals previously unnoticed correlations between developmental modules and patterns of phenotypic integration. We propose that the primary axes of morphological variation among East African cichlid adaptive radiations are constrained by the hierarchical modularity of the teleost head skeleton.

Highlights

Cichlid fishes from the Rift Lakes of East Africa have undergone the most spectacular adaptive radiations in vertebrate history
We examined the morphological divergence and craniofacial development of Copadichromis azureus (CA), which is an omnivorous cichlid with small jaws [37]; and Dimidiochromis compressiceps (DC), known as the “Malawi eye-biter,” which is a predator of small fishes with a large mouth and fast biting jaws [38]
In order to determine which aspects of skull anatomy contribute to the observed morphological differences, we quantified shape variation between CA and DC using a morphometric analysis where axes of significant divergence were identified by canonical variate analysis (CVA)

Summary

Introduction

Cichlid fishes from the Rift Lakes of East Africa have undergone the most spectacular adaptive radiations in vertebrate history. Eco-morphological adaptations in lakes Victoria, Malawi and Tanganyika have resulted in a vast array of skull shapes and sizes, yet primary axes of morphological variation are conserved in all three radiations, prominently including the size of the preorbital region of the skull This conserved pattern suggests that development may constrain the trajectories of cichlid head morphological evolution. A second set of genes including, but not limited to, jag1b, nkx3.2 and hand subdivides individual pharyngeal arches into dorsal, intermediate and ventral domains, respectively, that give rise to correspondingly located skeletal elements with specific shapes and sizes [18] The overlap of these two orthogonal patterning systems defines semiautonomous developmental modules through which individual skeletal elements could evolve independently from each other. The hierarchical modularity of the vertebrate head may provide useful clues to understanding how patterns of head evolution have been shaped by the developmental constraints imposed by this organization

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