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Home Range Overlap, Matrilineal and Biparental Kinship Drive Female Associations in Bottlenose Dolphins

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Home Range Overlap, Matrilineal and Biparental Kinship Drive Female Associations in Bottlenose Dolphins Animal Behaviour 80 (2010) 481e486 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins C.H. Frère a,*, M. Krützen a,b,1, J. Mann a,c,2, J.J. Watson-Capps d,3, Y.J. Tsai c,2, E.M. Patterson c,2, R. Connor a,e,4, L. Bejder f,5, W.B. Sherwin a a School of Biological Earth and Ecological Sciences, University of New South Wales b Anthropological Institute and Museum, University of Zürich c Departments of Biology and Psychology, Georgetown University d Biology Department, Metropolitan State College of Denver e Department of Biology, UMASS-Dartmouth f Centre for Fish and Fisheries Research, Division of Science and Engineering, Murdoch University article info Few studies of kinship in mammalian societies have been able to consider the complex interactions Article history: between home range overlap, association patterns and kinship, which have created a critical gap in our Received 9 December 2009 understanding of social evolution. We investigated the association patterns of female bottlenose Initial acceptance 28 January 2010 dolphins, Tursiops aduncus, in the eastern gulf of Shark Bay, Western Australia and found that they Final acceptance 4 June 2010 depended upon the complex interplay of at least three factors: home range overlap, matrilineal kinship Available online 14 July 2010 and biparental kinship. While home range overlap was positively correlated with female association MS. number: 09-00780R patterns, preferred associations were found between females showing as little as 27% home range overlap, and some pairs showed avoidance despite 100% home range overlap. Furthermore, on average, Keywords: both casual and preferred associations took place between females that were more closely biparentally bottlenose dolphin related than expected by chance and this pattern varied depending upon whether or not pairs of females home range shared the same matriline. HWI kinship Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. relatedness social evolution Tursiops aduncus The influence of inclusive fitness on affiliative behaviour has Parsons et al. 2003; Gero et al. 2009). Owing to practical difficulties been extensively studied in species ranging from eusocial insects in data collection, however, few studies of kinship in mammalian (Reeve et al. 1990; Seger 1991; Bourke 1997) to long-lived societies have been able to consider the complex interactions mammals such as primates (Chapais 2001; Clutton-Brock 2002; between home range overlap, association patterns and kinship Perry et al. 2008; Langergraber et al. 2009), lions, Panthera leo (Maher 2009). This represents a critical gap in our understanding of (Packer et al. 1991), elephants (Fernando & Lande 2000; Archie et al. social evolution. 2006) and cetaceans (Whitehead & Baird 2000; Krützen et al. 2003; Biparental relatedness (genetic relatedness measured from nuclear DNA) is clearly an important factor in affiliative behaviour and is central to the theory of kin selection (Hamilton 1964a, b). * Correspondence: C. H. Frère, School of Biological Earth and Ecological Sciences, There is also good reason to study maternal relatedness (genetic University of New South Wales, Sydney, NSW 2052, Australia. relatedness measured from mitochondrial DNA), especially when E-mail address: [email protected] (C.H. Frère). focusing on female association. For instance, Archie et al. (2006) 1 M. Krützen is at the Anthropological Institute and Museum, University of found that groups of African savannah elephants, Loxodonta afri- Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland. 2 J. Mann, Y. J. Tsai and E. M. Patterson are at the Departments of Biology and cana, that shared mtDNA haplotypes were more likely to fuse than Psychology, Georgetown University, Washington DC 20057-1229, U.S.A. groups that did not. Female bottlenose dolphins, Tursiops aduncus, 3 J. J. Watson-Capps is at the Biology Department, Metropolitan State College of in Port Stephens, Australia, were found to associate more with Denver, Denver, CO 80217, U.S.A. other females that shared the same mtDNA haplotype (Möller et al. 4 R. Connor is at the Department of Biology, UMASS-Dartmouth, Dartmouth, MA 2006). In the eastern gulf of Shark Bay, mtDNA analysis revealed 02747, U.S.A. 5 L. Bejder is at the Centre for Fish and Fisheries Research, Division of Science and that a particular foraging technique shared by several females and Engineering, Murdoch University, South Street, Murdoch, WA 6150, Australia. their offspring occurred almost exclusively within the same 0003-3472/$38.00 Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2010.06.007 482 C.H. Frère et al. / Animal Behaviour 80 (2010) 481e486 matriline (Mann & Sargeant 2003; Krützen et al. 2005; Sargeant the association estimates between pairs of females using the half- et al. 2005; Mann et al. 2008). Thus, the interpretation of the weight index (HWI), which is the most appropriate association results can depend upon whether biparental or matrilineal kinship index when members of each possible pair are more likely to be is investigated. scored when separate than when together (Cairns & Schwager When data are available, nongenetic factors, such as home range 1987). The half-weight index is defined as HWI x/{x y 0.5 ¼ þ ab þ overlap, should be included when investigating the role that (y y )}, where x number of encounters for which both dolphin a þ b ¼ matrilineal and biparental kinship play in mammalian societies. ‘a’ and ‘b’ were in the same group; y number of encounters a ¼ Space use and ranging patterns of individuals have commonly been including dolphin ‘a’ but not dolphin ‘b’ in the same group; used to investigate social structure. This is because the amount of y number of encounters including dolphin ‘b’ but not dolphin ‘a’ b ¼ spatial overlap between individuals provides indirect information in the same group; and y number of encounters including ab ¼ about the probability of social interactions (Clutton-Brock 1989). dolphin ‘a’ and ‘b’ in different clusters of groups at the same time For instance, association patterns among tent-making bats, Artibeus (Cairns & Schwager 1987). The HWI index ranges from 0 (never watsoni, correlate with roosting and foraging home range overlap seen together) to 1 (never seen apart). HWI estimates were calcu- (Chaverri et al. 2007). The degree of spatial overlap between female lated in SOCPROG 2.2 (Whitehead 1999). Second, only females and male marmots, Marmota monax, correlates with kinship sighted more than 30 times were included in the analysis. A high (Maher 2009). Home range overlap, however, does not always sighting number increases the chance of having captured all explicitly account for association patterns. Association patterns possible associates within a female’s social network. In our data set, among female grey kangaroos, Macropus giganteus, were not we found that the percentage of HWI equal to zero reached exclusively predicted by their patterns of spatial overlap (Carter a plateau above 30 sightings. This indicates that zero HWI estimates et al. 2009). Similarly, no correlation was found between female between pairs of females that have been sighted at least 30 times elephant core areas and their association patterns (De Villiers & Kok are more likely to be real ‘avoidances’ rather than the result of not 1997). having sampled those two females together. Except for the study by Möller et al. (2006) on the association The standard deviation and the coefficient of variation of HWI, patterns and kinship of female bottlenose dolphins in Port Ste- based on the observed distribution of HWI, were used as indication phens, interactions between relatedness and association patterns of the level of structure within the female social system (Whitehead have generally focused on male dolphins (e.g. Möller et al. 2001; 1999, 2009). Overall pairwise associations were tested for depar- Krützen et al. 2003, 2004a). Female bottlenose dolphins report- tures from randomness using the permutation procedure devel- edly form loose social bonds with other females of various ages and oped by Manly (1995) and available in SOCPROG 2.2. This degrees of kinship (Wells et al. 1987; Smolker et al. 1992; Möller permutation procedure (referred to as the MBFB method) was et al. 2006). In the eastern gulf of Shark Bay, the affiliation adapted for association data by Bejder et al. (1998) and redefined by patterns of female dolphins can be characterized as ‘resident- Whitehead (1999) to account for demographic effects. We ran egalitarian’ (in the sense of Sterck et al. 1997) based on the scarcity 20 000 permutations with 1000 flips per permutation for each of contest competition among females (Scott et al. 2005). While analysis, and significant variations from random were tested using female dolphin affiliation patterns do not show the same group a two-tailed test (a 0.05). The sampling period was set to 1 day to ¼ structure as those of males, they have a more labile open fis- avoid replication of association within the same day. sionefusion grouping pattern (Smolker et al. 1992). In contrast, To investigate further the interaction between associations and males form long-term alliances of up to 14 animals (Connor et al. biparental kinship, we subdivided HWI association estimates of 1992a, b, 2000, 2001) that sexually coerce females and compete each females into three categories: avoidance (A), casual (C) and to prevent other alliances from gaining access to females (Scott preference (P). Pairwise association estimates at or below the 2.5% et al. 2005; Connor et al. 2006). percentile were considered as avoidance (A). Pairwise association In this study, we used a combination of behavioural and genetic estimates at or above the 97.5% percentile were considered as data to explore the influence of both home range overlap and preference (P).
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