Ecomorphological divergence and habitat lability in the context of robust patterns of modularity in the cichlid feeding apparatus

Andrew J Conith,Michael R Kidd,Thomas D Kocher,R Craig Albertson

doi:10.1186/s12862-020-01648-x

Andrew J Conith, Michael R Kidd + Show 2 more

Open Access

https://doi.org/10.1186/s12862-020-01648-x

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Abstract

BackgroundAdaptive radiations are characterized by extreme and/or iterative phenotypic divergence; however, such variation does not accumulate evenly across an organism. Instead, it is often partitioned into sub-units, or modules, which can differentially respond to selection. While it is recognized that changing the pattern of modularity or the strength of covariation (integration) can influence the range or rate of morphological evolution, the relationship between shape variation and covariation remains unclear. For example, it is possible that rapid phenotypic change requires concomitant changes to the underlying covariance structure. Alternatively, repeated shifts between phenotypic states may be facilitated by a conserved covariance structure. Distinguishing between these scenarios will contribute to a better understanding of the factors that shape biodiversity. Here, we explore these questions using a diverse Lake Malawi cichlid species complex, Tropheops, that appears to partition habitat by depth.ResultsWe construct a phylogeny of Tropheops populations and use 3D geometric morphometrics to assess the shape of four bones involved in feeding (mandible, pharyngeal jaw, maxilla, pre-maxilla) in populations that inhabit deep versus shallow habitats. We next test numerous modularity hypotheses to understand whether fish at different depths are characterized by conserved or divergent patterns of modularity. We further examine rates of morphological evolution and disparity between habitats and among modules. Finally, we raise a single Tropheops species in environments mimicking deep or shallow habitats to discover whether plasticity can replicate the pattern of morphology, disparity, or modularity observed in natural populations.ConclusionsOur data support the hypothesis that conserved patterns of modularity permit the evolution of divergent morphologies and may facilitate the repeated transitions between habitats. In addition, we find the lab-reared populations replicate many trends in the natural populations, which suggests that plasticity may be an important force in initiating depth transitions, priming the feeding apparatus for evolutionary change.

Highlights

Adaptive radiations are characterized by extreme and/or iterative phenotypic divergence; such variation does not accumulate evenly across an organism
We focus on characterizing the feeding apparatus of Tropheops, as members of this species complex occupy a spectrum of depths from shallow sediment-free conditions that require a more robust feeding apparatus to pluck attached filamentous algae from rocks, to deep sediment-rich habitats that require a more gracile feeding apparatus to sift through sediment on and between the rocks [28, 38]
Tropheops phylogenetic tree Our Bayesian tree constructed using amplified fragment length polymorphism (AFLP) markers exhibited monophyletic groupings for the Tropheops and Maylandia species complexes within the mbuna (Figure S1; Table S1)

Summary

Introduction

Adaptive radiations are characterized by extreme and/or iterative phenotypic divergence; such variation does not accumulate evenly across an organism Instead, it is often partitioned into sub-units, or modules, which can differentially respond to selection. Repeated shifts between phenotypic states may be facilitated by a conserved covariance structure Distinguishing between these scenarios will contribute to a better understanding of the factors that shape biodiversity. Characterizing the pattern and magnitude of covariation among traits has been a central theme of evolutionary biology for more than 200 years [1, 2] It was not until Olson and Miller [3] that the understanding of trait covariation was formalized into a statistical framework. If regions of an organism can develop and evolve independently, this could permit an increase in morphological diversity (i.e., disparity [10]), open up unique or unoccupied niches [11], and influence the rate of evolution [7, 12]

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