Filogeografia e diversidade genética dos cachalotes Physeter macrocephalus Linnaeus, 1758 no Atlântico Sul Ocidental

Abstract

Sperm whales, Physeter macrocephalus Linnaeus, 1758, are widely distributed throughout the world's oceans. However, males and females have marked differences in their distribution pattern. Worldwide studies on genetics, ecology and vocal behavior comparing populations suggested the existence of a strong matrilineal social structure with female high philopatry in tropical regions, and gene flow mediated by males. The populations of the southwestern Atlantic Ocean (SWA) are still considered the least known and studied. In order to identify possible management units of the species in the SWA, the present study presented the first analysis of the genetic diversity and the evaluation of the potential structuring of the sperm whale populations along the SWA, using sequences from the mitochondrial DNA control region (mtDNA) of 565 bp obtained from samples collected in the region. In addition, it was also aimed to establish the phylogeographic relationships among these SWA populations and those of the rest of the world. Fifty-eight sperm whales from three geographic areas on the Brazilian coast (northeast = 15, southeast = 3, south = 36) and one from the coast of Argentina (n = 4) were analyzed and compared with 1577 sequences from other oceans and available in GenBank (Atlantic = 362, Indian = 159 and Pacific = 1056). In addition, the sex of 39 specimens was molecularly determined in order find females outside of the northeastern coast of Brazil, which would confirm the existence of more than one sperm whale population in the SWA. The analysis of mtDNA sequences revealed the existence of four genetic groups and seven haplotypes in SWA. The haplotype (Hd) and nucleotide (π) diversities observed for the species as a whole in SWA were Hd = 0.6824 e π = 0.002296, respectively. The selective neutrality tests did not suggest significant changes in the effective population size or recent population expansion for the species in SWA. The results of the molecular analysis of variance (AMOVA) revealed that between 9.14% (ΦST) and 12.31% (FST) of the genetic diversity variation observed are due to differences between populations. However, this geographical differentiation was only significant between the populations of northeast and southeast-south Brazil, which had the highest fixation index between them (northeast and southeast-south Brazil: FST = 0.1089, ΦST = 0.1378; northeast Brazil and Argentina: FST = - 0.1076; ΦST = - 0.0512; southeast-south of Brazil and Argentina: FST=0.0742; ΦST=0.1206; P<0.00001). The population of northeastern Brazil had the lowest genetic diversity of the study (Hd = 0.5128 and π = 0.001796), when compared to the southeast-south populations (Hd = 0.6659 and π = 0.002482), and Argentina (Hd = 0.8333 and π = 0.002043). The southeast-south coast of Brazil presented three exclusive haplotypes in a total of seven, while the coast of Argentina presented a particular haplotype. Only the samples from the southeast-south region of Brazil presented an exclusive genetic group, suggesting that the distribution of the genetic variation is better understand with the existence of three groups of sperm whales along the SWA (northeast of Brazil, southeast-south of Brazil and Argentina), which could be considered as different management units. Regarding the worldwide genetic structure of sperm whales, 39 haplotypes and four genetic groups were recovered, and only the Pacific Ocean presented an exclusive genetic group. AMOVA revealed that between 8.89% (FST) and 16.39% (ΦST) of the observed genetic variation was due to differences among the populations of the world. AMOVA indicated that there is a geographical differentiation between the SWA and the other oceans, which had high indexes of fixation between them (SWA and North Atlantic: FST = 0.1837, ΦST = 0.3142, SWA and Indian Ocean: FST = 0.0898; ΦST = 0.1661; SWA and Pacific: FST = 0.11140; ΦST = 0.0757; P<0.00001). The unified sample of the SWA did not present exclusive haplotypes. However, individuals from the southeast-south of Brazil only shared six of seven haplotypes with the population of the Pacific Ocean. From 39 sperm whales with sex molecularly determined, nine were males and 30 females, 18 females were found in the southern region, outside the tropical region, suggesting that there are at least more than one reproductive population in WSA. These results, together with the differences in genetic variability and the lack of sharing of haplotypes among the studied populations, suggest that sperm whales from southeast-south of Brazil would be a management unit, potentially isolated, in reproductive terms, from the others. However, mtDNA is a matrilineal marker and exclusively presents the evolutionary history of females. In this context, the continuity of these studies, including new samples and nuclear markers, will be fundamental for the identification of real units of management of the species in the SWA and particularly in Brazilian waters.