Temperature and oxygen levels drive the evolution of morphological, behavioral, and physiological traits in marine invertebrates, including crustaceans. Environmental conditions are also expected to prompt the adaptive evolution of mitochondrial protein-coding genes (PCGs), which are vital for energy production via the oxidative phosphorylation pathway. We formally tested for adaptive evolution in mitochondrial protein-coding genes in representatives of the decapod infraorder Achelata, including two spiny lobsters, Panulirus echinatus and Panulirus interruptus, for which we sequenced complete mitochondrial genomes (15,644 and 15,659 bp long, respectively). A phylomitogenomic analysis based on all 13 mitochondrial PCGs for 24 species belonging to the infraorder Achelata, plus an outgroup representing the infraorders Caridea and Nephropidae, supported the monophyly of the genus Panulirus, the families Palinuridae and Scyllaridae, and the infraorder Achelata. Over the strong negative selection background observed for mitochondrial PCGs in the Achelata, signatures of positive selective pressure were detected within PCGs in equatorial Panulirus spp. and deepwater Scyllaridae. In Panulirus spp. inhabiting equatorial latitudes with consistently high temperatures, the Datamonkey analysis RELAX suggested intensified purifying selection strength in 9 of the 13 PCGs and relaxation in purifying selection strength in atp6, while aBSREL, BUSTED, and MEME recovered signatures of positive selection on PCGs within Complex I, III, and IV PCGs. Likewise, in Scyllaridae species inhabiting depths with low oxygen levels, RELAX indicated relaxed selection strength in 6 of the 13 PCGs, while aBSREL, BUSTED, and MEME recovered signatures of positive selection on PCGs within Complexes I, III, IV, and V. Adaptive evolution likely retains mutations that improve protein stability at sustained temperatures and enhance mitochondrial capacity for energy metabolism in low oxygen conditions. These mutations likely optimize the ability of Complex I to pump protons into the mitochondrial intermembrane space, improve electron transfer and proton translocation in Complex III, boost the efficiency with which Complex IV transfers electrons to oxygen to form water, and refine the ability of Complex V to produce energy via oxidative phosphorylation. The newly assembled mitochondrial genomes of P. echinatus and P. interruptus represent new genomic resources to aid the conservation and management of lobsters targeted by major fisheries through applications such as bioprospecting using eDNA sampling and species identification via DNA barcoding. This study also contributes to our understanding of how environmental conditions drive adaptive evolution in spiny and slipper lobster mitochondrial PCGs and supports the notion that mitochondrial protein-coding genes can and do experience adaptive evolution to optimize mitochondrial function in a wide variety of organisms. Further research is needed to clarify which and how environmental conditions influence the adaptive evolution of mitochondrial PCGs in other crustacean lineages and beyond.
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