Long Distance Runners in the Marine Realm: New Insights Into Genetic Diversity, Kin Relationships and Social Fidelity of Indian Ocean Male Sperm Whales

Abstract

Adult male sperm whales (Physeter macrocephalus) are long distance runners of the marine realm, feeding in high latitudes and mating in tropical and subtropical waters where stable social groups of females and immatures live. Several areas of uncertainty still limit our understanding of their social and breeding behavior, in particular concerning the potential existence of geographical and/or social fidelities. In this study, using underwater observation and sloughed-skin sampling, we looked for male social fidelity to a specific matrilineal sperm whale group near Mauritius. In addition, we captured a wider picture of kin relationships and genetic diversity of male sperm whales in the Indian Ocean thanks to biopsies of eight individuals taken in a feeding ground near the Kerguelen and Crozet Archipelagos (Southern Indian Ocean). Twenty-six adult male sperm whales were identified when socializing with adult females and immatures off Mauritius. Sloughed-skin samples were taken from thirteen of them for genetic analysis. Long-term underwater observation recorded several noteworthy social interactions between adult males and adult females and/or immatures. We identified seven possible male recaptures over different years (three by direct observation, and four at the gametic level), which supports a certain level of male social fidelity. Two probable first- and thirty second-degree kin relationships were highlighted between members of the social unit and adult males, confirming that some of the adult males observed in Mauritian waters are reproductive. Male social philopatry to their natal group can be excluded, as none of the males sampled shared the haplotype characteristic of the matrilineal social group. Mitochondrial DNA control region haplotype and nucleotide diversities calculated over the 21 total male sperm whales sampled were similar to values found by others in the Indian Ocean. Our study strongly supports the existence of some levels of male sperm whale social fidelity, not directed to their social group of birth, in the Indian Ocean. Males sampled in breeding and feeding grounds are linked by kin relationships. Our results support a model of male mediated gene flow occurring at the level of the whole Indian Ocean, likely interconnected with large-scale geographical fidelity to ocean basin, and a small-scale social fidelity to matrilineal social groups.

A piece of the puzzle: analyses of recent strandings and historical records reveal new genetic and ecological insights on New Zealand sperm whales

“…We identified 7 mtDNA haplotypes among the 14 whales, including 1 haplotype ('New') that had not been previously described, including among novel haplotypes recently described by Day et al (2021) and Girardet et al (2022) (Fig. 2).…”

“…To compare the mtDNA haplotypes found among New Zealand males with diversity elsewhere, we aligned our sequences with haplotypes from Alexander et al (2016), Girardet et al (2022) and Day et al (2021) using the Geneious 9.0.5 algorithm. Haplotypes unique over a 624 bp consensus region (ignoring missing data at the beginning/end of sequences), corresponding to the start of GenBank sequences MT939514−MT939515 from Day et al (2021) and the end of KU719571 from Alexander et al (2016), were exported in nexus format (see Supplement 2 Alignment_including_IO_network.nex) and used to construct a haplotype network using the median-joining method (Bandelt et al 1999) in Pop -Art (Leigh & Bryant 2015).…”

“…Haplotype frequency information collated from Alexander et al (2016), Day et al (2021), Girardet et al (2022) (and references therein) was used: (1) to visualise haplotype frequency differences between the 2018 Taranaki male strandings and other regions within the Indian and Pacific Oceans (using haplo-type_data.txt provided in Supplement 2 as input) and…”

“…We carried out similar broad-scale comparisons using haplotype frequency as those investigated for the haplotype network. In addition, we used the regional areas within the Indian Ocean, Pacific Ocean and Australia defined by previous publications (Alexander et al 2016, Day et al 2021, Girardet et al 2022 to investigate geographic affinities at a finer scale.…”

“…In contrast, males disperse from their natal groups, and bachelor groups have long been thought to be comprised exclusively of non-related individuals. However, recent genetic evidence suggests that related males may be found within at least some bachelor groups (Girardet et al 2022).…”