Shared ecological traits influence shape of the skeleton in flatfishes (Pleuronectiformes)

Abstract

In the age of phylogenetic comparative methods, evolutionary biologists have been able to explore evolutionary trends in form in unique and extraordinarily diverse groups of animals. Pleuronectiformes, commonly known as flatfishes, is a diverse and specialized order of fishes that have remarkable asymmetry induced by ocular migration and a benthic life style. Although flatfishes are unique from other fishes, species within the group are morphologically diverse. The origin of ocular migration has been a primary focus of research; however, little is known about overall shape diversification among the flatfishes. In this study, we use integrative methods to examine how body shape evolved within the flatfishes. Shape was quantified from X-rays using geometric morphometrics for 389 individuals across 145 species. The most recent and robust phylogeny was overlaid onto the morphospace and phylogenetic signal was calculated to ascertain convergence in the morphospace. In addition, phylogenetic linear models were employed to determine if ecological traits were correlated with shape and if size had an effect on overall body shape. Results revealed that the majority of variation evolved recently, within the past 15-10-million-years in the middle Miocene, and is highly variable within the flatfishes. These changes are best summarized by body depth, jaw length and medial fin length. Dorsal and anal fin length are correlated, which may be due to the unique mode of locomotion used by flatfishes. A phylogenetic linear model and phylomorphospace analysis suggested that several ecological traits are correlated with shape, which indicates an ecological role in the diversification of flatfishes.

Keywords: Body shape; Comparative methods; Ecology; Fish; Geometric morphometrics; Marine; Morphological evolution.

Figure 1. Diversity of skeletal morphology in the flatfishes.

(A) Achirus lineatus (Achiridae); (B) Lyopsetta exilis (Pleuronectidae); (C) Plagiopsetta glossa (Samaridae); (D) Psettodes belcheri (Psettodidae); (E) Rhombosolea plebeia (Pleuronectidae); (F) Gymnachirus melas (Achiridae); (G) Symphurus plagiusa (Cynoglossidae); (H) Syacium micrurum (Paralichthyidae); (I) Lepidorhombus boscii (Scophthalmidae); and (J) Scophthalmus maximus (Scophthalmidae). Gray bars represent a 1 cm scale.

Figure 2. Body shape variation within flatfishes.

The morphospace biplot of PCs 1 and 2 represents 74.2% of the body shape variation within the flatfishes. Each point indicates the mean of a species with colors matching the family depicted in the key. Backtransformed shapes (in gray) portray shape variation throughout morphospace with fin length, jaw length and spinal curvature represented as black lines on shapes.

Figure 3. Phylomorphospace of body shape within flatfishes.

The genomic phylogeny (Byrne, Chapleau & Aris-Brosou, 2018) projected onto the morphospace to demonstrate the evolutionary relationships of body shape variation within the flatfishes. Solid colored points indicate the mean of a species with ancestral nodes represented by small white circles.

Figure 4. Chronophylomorphospace of body shape within flatfishes.

The time-calibrated genomic phylogeny (Byrne, Chapleau & Aris-Brosou, 2018) mapped onto the morphospace with the time in millions of years depicted on the z-axis. Colored points indicate the mean of a species and the black arrow indicates the root of the phylogeny. A two-dimensional morphospace is represented as a shadow at the bottom of the graph.

Figure 5. Relationship of body shape and size in flatfishes.

(A) Scatterplot of the regression of body shape on the log centroid size and (B) the predicted shape values from regression scores for each family. Each dot indicates the mean of a species with colors coordinating to the family depicted in the key.