Insights into the Mitochondrial Genetic Makeup and Miocene Colonization of Primitive Flatfishes (Pleuronectiformes: Psettodidae) in the East Atlantic and Indo-West Pacific Ocean

Abstract

The mitogenomic evolution of the Psettodes flatfishes is still poorly known from their range distribution in eastern Atlantic and Indo-West Pacific Oceans. The study delves into the matrilineal evolutionary pathway of these primitive flatfishes, with a specific focus on the complete mitogenome of the Psettodes belcheri species, as determined through next-generation sequencing. The mitogenome in question spans a length of 16,747 base pairs and comprises a total of 37 genes, including 13 protein-coding genes, 2 ribosomal RNA genes, 22 transfer RNA genes, and a control region. Notably, the mitogenome of P. belcheri exhibits a bias towards AT base pairs, with a composition of 54.15%, mirroring a similar bias observed in its close relative, Psettodes erumei, which showcases percentages of 53.07% and 53.61%. Most of the protein-coding genes commence with an ATG initiation codon, except for Cytochrome c oxidase I (COI), which initiates with a GTG codon. Additionally, four protein-coding genes commence with a TAA termination codon, while seven others exhibit incomplete termination codons. Furthermore, two protein-coding genes, namely NAD1 and NAD6, terminate with AGG and TAG stop codons, respectively. In the mitogenome of P. belcheri, the majority of transfer RNAs demonstrate the classical cloverleaf secondary structures, except for tRNA-serine, which lacks a DHU stem. Comparative analysis of conserved blocks within the control regions of two Psettodidae species unveiled that the CSB-II block extended to a length of 51 base pairs, surpassing the other blocks and encompassing highly variable sites. A comprehensive phylogenetic analysis using mitochondrial genomes (13 concatenated PCGs) categorized various Pleuronectiformes species, highlighting the basal position of the Psettodidae family and showed monophyletic clustering of Psettodes species. The approximate divergence time (35-10 MYA) between P. belcheri and P. erumei was estimated, providing insights into their separation and colonization during the early Miocene. The TimeTree analysis also estimated the divergence of two suborders, Psettodoidei and Pleuronectoidei, during the late Paleocene to early Eocene (56.87 MYA). The distribution patterns of Psettodes flatfishes were influenced by ocean currents and environmental conditions, contributing to their ecological speciation. In the face of climate change and anthropogenic activities, the conservation implications of Psettodes flatfishes are emphasized, underscoring the need for regulated harvesting and adaptive management strategies to ensure their survival in changing marine ecosystems. Overall, this study contributes to understanding the evolutionary history, genetic diversity, and conservation needs of Psettodes flatfishes globally. However, the multifaceted exploration of mitogenome and larger-scale genomic data of Psettodes flatfish will provide invaluable insights into their genetic characterization, evolutionary history, environmental adaptation, and conservation in the eastern Atlantic and Indo-West Pacific Oceans.

Keywords: ancient lineages; evolution; marine fish; mitogenome; oceanography; phylogeny.

Figure 1

Global distribution of Pleuronectiformes along with the ocean surface currents (warm and cold currents are marked by the red and blue arrow, respectively). Collection locality of Psettodes belcheri is marked by a red pin from Cameroon, Africa. The .shp files were acquired from the IUCN database (accessed on 15 August 2023). The species photographs were taken by the sixth author (F.Z.G) and edited manually in Adobe Photoshop CS 8.0.

Figure 2

The mitochondrial genome of Psettodes belcheri drawn by the MitoAnnotator online server. PCGs, rRNAs, tRNAs, and CR are indicated by different color arcs. The species photographs were taken by the sixth author (F.Z.G) and edited manually in Adobe Photoshop CS 8.0.

Figure 3

Secondary structures of 22 transfer RNAs (tRNAs) of P. belcheri display the structural variation. The tRNAs are denoted by full names and IUPAC-IUB single-letter amino acid codes. The first structure shows the nucleotide positions and details of the stem–loop of tRNAs. Watson–Crick and wobble base pairing are marked by black and red color bars, respectively.

Figure 4

(A) Comparison of length and nucleotide composition of four conserved domains of two Psettodes species control regions. The variable nucleotides are marked in stars; (B) The gene arrangements of two Psettodes species mitogenomes.

Figure 5

The Bayesian matrilineal phylogeny based on the concatenated sequences of 13 PCGs exhibits the evolutionary relationship of Psettodes species with other Pleuronectiformes. The Bayesian posterior probability values are displayed with each node.

Figure 6

The maximum-likelihood-based TimeTree elucidates the approximate divergence time of the Psettodes species along with other Pleuronectiformes species. The approximate divergence times are marked displayed with each node. The red squares represent the calibration points obtained from the prior work [26].

Figure 7

(A) Maps displaying the maritime environments during the Eocene and Miocene periods (source: Encyclopædia Britannica, Inc.). Schematic representation of the major current systems, as defined by the International Group for Marine Ecological Time Series, in the North Atlantic, South Atlantic, and Indo-West Pacific regions. This section also explores the potential diversification and colonization of primitive flatfishes: (B) P. bennettii, (C) P. belcheri, and (D) P. erumei. The illustration of the Psettodes species was sourced from the free media repository (Wikimedia Commons), as well as a previous study [33]. The maps were generated using the DIVA-GIS platform, utilizing IUCN range distribution data (.shp files). Additionally, the illustration of ocean currents is based on insights from a previous study [94]. Violet arrows indicate the warmer currents, while the blue arrows signify the cooler currents.