The evolutionary history of manatees told by their mitogenomes

Abstract

The manatee family encompasses three extant congeneric species: Trichechus senegalensis (African manatee), T. inunguis (Amazonian manatee), and T. manatus (West Indian manatee). The fossil record for manatees is scant, and few phylogenetic studies have focused on their evolutionary history. We use full mitogenomes of all extant manatee species to infer the divergence dates and biogeographical histories of these species and the effect of natural selection on their mitogenomes. The complete mitochondrial genomes of T. inunguis (16,851 bp), T. senegalensis (16,882 bp), and T. manatus (16,882 bp), comprise 13 protein-coding genes, 2 ribosomal RNA genes (rRNA - 12S and 16S), and 22 transfer RNA genes (tRNA), and (D-loop/CR). Our analyses show that the first split within Trichechus occurred during the Late Miocene (posterior mean 6.56 Ma and 95% HPD 3.81–10.66 Ma), followed by a diversification event in the Plio-Pleistocene (posterior mean 1.34 Ma, 95% HPD 0.1–4.23) in the clade composed by T. inunguis and T. manatus; T. senegalensis is the sister group of this clade with higher support values (pp > 0.90). The branch-site test identified positive selection on T. inunguis in the 181st position of the ND4 amino acid gene (LRT = 6.06, p = 0.0069, BEB posterior probability = 0.96). The ND4 gene encodes one subunit of the NADH dehydrogenase complex, part of the oxidative phosphorylation machinery. In conclusion, our results provide novel insight into the evolutionary history of the Trichechidae during the Late Miocene, which was influenced by geological events, such as Amazon Basin formation.

First Description of a Satellite DNA in Manatees’ Centromeric Regions

“…In T. inunguis , we confirmed the presence of TMAsat by PCR and FISH and despite the two species having different karyotypes (2 n =48 and 2 n =56, respectively), TMAsat displayed the same chromosome localization ( Figure 2 ). This could be related to the recent ~1.34 million years ago (Mya) divergence time between the species ( de Souza et al, 2021 ).…”

“…Nevertheless, we cannot discard a species-specific TMAsat sequence in T. inunguis since some mutations are present in all or almost all five sequences and are absent or present in just few monomers outside the species. West Indian and Amazonian manatees present a recent divergence time ( de Souza et al, 2021 ) and an incomplete reproductive isolation ( Vianna et al, 2006 ; Lima et al, 2019 ), which could contribute to the TMAsat high interspecific homogeneity observed. Overall, the species-specific mutations of the group are probably not yet fixed, despite the ~46.83 Mya estimated split of Trichechidae and Dugongidae, thus lacking species-specific sequences as reflected in the neighbor joining tree ( Figure 3D ), which disagrees with the predictions of concerted evolution.…”

“…TMAsat monomers from T. manatus , T. inunguis , D. dugon , and H. gigas lack species-specific sequences, contradicting the predictions of concerted evolution. The TMAsat-like ancestral sequence is present in other Paenungulata, such as elephants and hyraxes, suggesting that TMAsat suffered an expansion within Sirenia less than ~69 Mya ( Foley et al, 2016 ; de Souza et al, 2021 ), after the divergence of Sirenia from Proboscidea and Hyracoidea.…”

Total evidence time-scaled phylogenetic and biogeographic models for the evolution of sea cows (Sirenia, Afrotheria)

“… All five taxa are represented by DNA sequences. Cladogram of molecular phylogenetic relationships is a composite from Springer et al (2015) and de Souza et al (2021) . Species distribution maps are adapted from the IUCN (2021) Red List of Threatened Species and from empirical H. gigas occurrence localities included in this study.…”

“…Although the pattern of descent among living manatees and dugongs (plus Steller’s sea cow) can now be considered well-resolved, molecular-based models that have estimated the timing of lineage divergences have yielded wildly different ages for the Dugongidae-Trichechidae split ( i.e ., crown Sirenia) and the Dugong-Hydrodamalis split ( i.e ., crown Dugongidae sensu this study; see Results). Estimates for the age of crown Sirenia range from middle Eocene (~46.8 Ma, de Souza et al, 2021 ; ~41.5 Ma, Springer et al, 2015 ; ~41 Ma, Plön et al, 2019 ), to Oligocene (~31.4 Ma, Meredith et al, 2011 ; ~30.9 Ma, Heritage, Seiffert & Borths, 2021 ), to Miocene (~16.6 Ma, Poulakakis & Stamatakis, 2010 ; ~13 Ma, Upham, Esselstyn & Jetz, 2019 ; ~5.74 Ma, Phillips, 2016 ), while estimates for the Dugong-Hydrodamalis split range from Oligocene (~29 Ma, Plön et al, 2019 ; ~28.6 Ma, Springer et al, 2015 ) to Miocene (~15.1 Ma, Heritage, Seiffert & Borths, 2021 ). These disparate evolutionary timescales have dramatically different implications for interpretations of the sirenian fossil record, including clade membership and biogeography.…”