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Keywords:

  • dispersal;
  • dolphins;
  • genetic relatedness;
  • social evolution;
  • toothed whales

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

Social systems are the outcomes of natural and sexual selection on individuals’ efforts to maximize reproductive success. Ecological conditions, life history, demography traits and social aspects have been recognized as important factors shaping social systems. Delphinids show a wide range of social structures and large variation in life history traits and inhabit several aquatic environments. They are therefore an excellent group in which to investigate the interplay of ecological and intrinsic factors on the evolution of mammalian social systems in these environments. Here I synthetize results from genetic studies on dispersal patterns, genetic relatedness, kin associations and mating patterns and combine with ecological, life history and phylogenetic data to predict the formation of kin associations and bonding in these animals. I show that environment type impacts upon dispersal tendencies, with small delphinids generally exhibiting female-biased philopatry in inshore waters and bisexual dispersal in coastal and pelagic waters. When female philopatry occurs, they develop moderate social bonds with related females. Male bonding occurs in species with small male-biased sexual size dimorphism and male-biased operational sex ratio, and it is independent of dispersal tendencies. By contrast, large delphinids, which live in coastal and pelagic waters, show bisexual philopatry and live in matrilineal societies. I propose that sexual conflict favoured the formation of these stable societies and in turn facilitated the development of kin-biased behaviours. Studies on populations of the same species inhabiting disparate environments, and of less related species living in similar habitats, would contribute towards a comprehensive framework for the evolution of delphinid social systems.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

Social systems epitomize the outcomes of natural and sexual selection on the attempts of individuals to maximize their inclusive fitness. In mammals, because of differences in the potential rate of reproduction (PRR) of males and females, the lifetime reproductive success of females is generally limited by food resources, while that of males is mainly constrained by access to mates (Trivers 1972; Emlen & Oring 1977; Clutton-Brock & Parker 1992). Female distribution is therefore mainly influenced by food abundance and distribution, while the distribution and number of females, and the presence and behaviour of other males, are expected to affect male distribution (Wrangham 1980). Ecological factors, primarily food distribution and predation risk, have been identified as the major causes of variation in mammalian social organization and structure (Rubenstein & Wrangham 1986).

In addition to ecological conditions, life history traits, demography and social factors related to intra-sexual competition and inter-sexual conflict are recognized as key factors shaping social systems (e.g. Bekoff et al. 1981; Sterck et al. 1997; Kappeler 1999; Clutton-Brock 2007; Bro-Jørgensen 2011), and these may also associate with phylogenetic signals (e.g. Di Fiore & Rendall 1994; Linklater 2000; Chapman & Rothman 2009). Among demographic factors, dispersal patterns have an important effect on social structure and social relationships. In mammals that live in social groups, females generally remain in their natal group or range, while males disperse before breeding (Greenwood 1980; Clutton-Brock & Lucas 2011). Because of their PRR, females benefit more than males from a high degree of familiarity with food resources, and this may be best attained by philopatry (Pusey & Packer 1987; Clutton-Brock & Lucas 2011). For males, sex differences in parental investment generally lead to a bias in the ratio of sexually receptive females to sexually mature males (the operational sex ratio, OSR), which in turn generates intensive competition among males for mates (Trivers 1972; Emlen & Oring 1977; Clutton-Brock & Parker 1992, 1995). Sexual conflict between females and males may then lead to sexual coercion of females by males (Van Schaik & Kappeler 1997; Kappeler 1999), which in turn promotes counter-strategies by females (Agrell & Wolff 1998). The interplay of social structure, dispersal patterns and mating tactics has important effects on the genetic structure of populations (Sugg et al. 1996; Dobson et al. 1998; Storz 1999), and in turn genetic relationships between individuals within populations are expected to influence their cooperative behaviours (Dobson et al. 1998).

Delphinid cetaceans are long-lived mammals that show a wide range of social structures, display large variation in life history traits and inhabit numerous marine, estuarine and freshwater environments (Wells et al. 1980, 1999; Connor 2000; Gowans et al. 2008). Some species of delphinids exhibit extremely complex social groupings matched only by other long-lived, large-brained mammals, such as primates and elephants (Connor et al. 1998). Delphinids are therefore an excellent group in which to investigate the interplay of ecological and intrinsic factors on the evolution of mammalian social systems in aquatic environments.

Recently, Gowans et al. (2008) proposed a socio-ecological model that considered the effects of food distribution, predation risk and ranging patterns on the evolution of delphinid social structure. This framework only considered the effects of ecological factors on social strategies, without taking into account the potential impacts of phylogeny, demography, life history traits and social factors on delphinid sociality. In this study I synthetize results from recent genetic studies on dispersal patterns, genetic relatedness, kin associations and mating patterns in delphinids and combine with ecological, life history and phylogenetic data to make predictions about the formation of kin associations and bonding in these animals. This represents an important step towards a more comprehensive framework for the evolution of social systems in delphinids.

The social structure of delphinids

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

Delphinids live in schools of a few individuals to thousands of animals, and these can range from very fluid schools of small delphinids to highly stable matrilineal pods of toothed whales that join up to form social groups at higher hierarchical levels (Table 1). Here I synthetize some of this variation with examples from the most studied species with different life histories and inhabiting disparate environments. Environments are classified according to Wells et al. (1999). ‘Inshore’ environments include enclosed bays and estuaries, and their associated coastal waters; ‘coastal’ as habitats along an open shoreline; and ‘pelagic’ as offshore deep-water habitats, including continental shelf waters, unbounded by shorelines.

Table 1.   Social structure in delphinids
SubfamilySpeciesSocial structureAssociation patternsGeneral bondsSex-specific bondsMean group sizeEnvironmentOcean regionReferences
  1. Studies were included if provided information on social structure, association patterns and group size of a particular population(s).

  2. Following McGowen (2011).

  3. §Individuals sighted ≥2 times were used for calculating association indices.

  4. Midway and Kure atolls, geographically isolated.

  5. ††Doubtful Sound, New Zealand, geographically isolated.

  6. ‡‡Individuals sighted ≥3 times were used for calculating association indices.

  7. §§Median group size.

LissodelphininaeCephalorhynchus commersoniiFission–fusionFluidWeak to moderate§ 2CoastalSouthwest AtlanticCoscarella et al. (2010, 2011)
Cephalorhynchus hectoriFission–fusionFluidWeak 2 to 8CoastalSouth PacificSlooten & Dawson (1988), Slooten et al. (1993) and Bräger (1999)
Lagenorhynchus obscurusFission–fusionFluidWeak with a few strong 7 to 10Coastal and pelagicSouthwest Atlantic and South PacificWürsig & Würsig (1980) and Pearson (2009)
Sotalia guianensisFission–fusionFluidWeak 12InshoreSouthwest AtlanticSantos & Rosso (2008)
DelphininaeStenella longirostrisFission–fusionFluidWeak with a few strongPossibly male coalitions35 to >100Pelagic (inshore for resting)North PacificWürsig et al. (1994) and Norris & Johnson (1994)
Bisexually bondedStableStrong, long term 211Pelagic (inshore for resting)North PacificKarczmarski et al. (2005)
Tursiops aduncusFission–fusionFluidWeak with some moderate and strongMale alliances/coalitions, female networks/clusters4 to 7InshoreEast Indian and Southwest PacificSmolker et al. (1992), Connor et al. (1992, 1999, 2011), Möller et al. (2001, 2002, 2006) and Wiszniewski et al. (2010, accepted)
Tursiops truncatusFission–fusionFluidWeak with some moderate and strongMale alliances, female bands5InshoreGulf of MexicoWells et al. (1987), Wells (1991) and Bouveroux & Mallefet (2010)
Fission–fusionFluidWeak with some moderate and strongMale alliances, moderate female bonds3 to 5CoastalNorth AtlanticRossbach & Herzing (1999) and Rogers et al. (2004)
Fission–fusionFluidWeak 20CoastalNortheast PacificDefran & Weller (1999)
Bisexually bondedStableStrong, long termBisexual bonds, possibly male coalitions17Inshore (Fjord)††South PacificLusseau et al. (2003) and Lusseau (2007)
Sousa chinensisFission–fusionFluidWeak 4 to 7Coastal and inshoreSouthwest Pacific and Southwest IndianKarczmarski (1999) and Parra et al. (2011)
Steno bredanensisFission–fusionFluidWeak to moderate‡‡ 7§§PelagicNorth PacificBaird et al. (2008b)
Orcaella heinsohniFission–fusionStableStrong, long term 5Coastal and inshoreSouthwest PacificParra et al. (2011)
GlobicephalinaeGrampus griseusSexually stratifiedStable/StratifiedStrong, long termMale clusters and female clusters13PelagicNorth AtlanticHartman et al. (2008)
Feresa attenuataBisexually bondedStableStrong, long termBisexual bonds13§§PelagicNorth PacificMcSweeney et al. (2009)
Globicephala melasMatrifocalStable/hierarchicalStrong, long termBisexual bonds14 to 20PelagicNorth Atlantic and Strait of GibraltarAmos et al. (1991, 1993), Ottensmeyer & Whitehead (2003) and de Stephanis et al. (2008)
Pseudorca crassidens StableStrong, long term 15§§PelagicNorth PacificBaird et al. (2008a)
Orcinus orcaMatrifocalStable/hierarchicalStrong, long termBisexual bonds2 to 9Coastal and pelagicNortheast and northwest PacificBigg et al. (1990), Baird & Dill (1996), Baird (2000), Ivkovich et al. (2009) and Parsons et al. (2009)

Small delphinids inhabiting inshore and coastal shallow waters are generally found in small schools, where school size and composition can change frequently (e.g. Wells et al. 1987; Smolker et al. 1992; Slooten et al. 1993; Bräger 1999). Depending on the availability of food resources, these dolphins may exhibit small home ranges and show year-round site fidelity, or larger range patterns and seasonal or weak site fidelity (e.g. Wells et al. 1987; Karczmarski 1999; Möller et al. 2002; Bräger et al. 2003). Sex and age segregation in small delphinids appears to repeatedly occur either between schools or within schools, depending on school size and activity, and the reproductive status of individuals (e.g. Wells et al. 1987; Smolker et al. 1992; Karczmarski 2000; Möller & Harcourt 2008). In all delphinids studied so far, the strongest social bonds are found between mothers and their calves. Apart from those, associations between some individuals persist more than with others. Strong and long-term social bonds have been particularly observed between male bottlenose dolphins (Tursiops spp.) and moderate bonds between females (Wells et al. 1987; Connor et al. 1992; Smolker et al. 1992; Möller et al. 2001, 2006; Wiszniewski et al. accepted). Other small delphinids, such as humpback dolphins (Sousa chinensis) and Hector’s dolphins (Cephalorhynchus hectori) living in coastal environments, appear to mainly exhibit casual and short-lasting affiliations between individuals (other than mother–calf pairs; Slooten et al. 1993; Bräger 1999; Karczmarski 1999; Karczmarski et al. 2000).

Small delphinids inhabiting deeper coastal waters are generally found in larger and more fluid schools than those found in inshore and shallow coastal waters. They also appear to have larger home ranges and show either little or seasonal site fidelity to local areas. In pelagic waters, they are found in medium-sized to extremely large schools reaching up to thousands of individuals; schools are dynamic in size and composition and are believed to range over vast areas (e.g. spotted and spinner dolphins in the eastern tropical Pacific; Scott & Cattanach 1998; Scott & Chivers 2009). Some degree of sex segregation within the large pelagic schools has also been proposed (e.g. Dohl et al. 1986; Pryor & Kang Schallenberger 1991).

In contrast, large delphinids, such as killer whales and long-finned pilot whales, living in coastal and offshore waters are found in smaller and more stable schools than those of small delphinids living in comparable environments and form hierarchically structured, matrilineal societies (Bigg et al. 1990; Amos et al. 1993). In addition, the Risso’s dolphin (Grampus griseus), a medium-sized delphinid that inhabits pelagic waters, appears to have a unique social structure, with stable long-term bonds organized in pairs or small clusters stratified by age and sex classes (Hartman et al. 2008).

The delphinid socio-ecological model

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

The risk of predation has long been suggested as one of the most important driving forces in the evolution of delphinid social organization (Norris & Dohl 1980; Norris & Schilt 1988), with school size generally associated with habitat openness, which in turn is correlated with the risk of predation (Wells et al. 1999). It is also well recognized that the distribution and abundance of food resources influence delphinid ranging patterns and school sizes and that cooperative foraging possibly played a role in the evolution of social organization in several species (Würsig 1986; Wells et al. 1999; Connor 2000). Detailed reviews of the potential benefits and costs of group living in odontocetes can be found in Wells et al. (1980, 1999), Connor (2000) and Gowans et al. (2008).

The delphinid socio-ecological model of Gowans et al. (2008) predicts that temporally and spatially predictable resources, which generally occur in complex inshore environments, should lead to high site fidelity, small home ranges and small school sizes. It further predicts the formation of female nursery groups for calf protection from predators, loose social networks of females based on reproductive status and long-term bonds between males for sequestering individual females for mating. By contrast, the framework envisages that when resources are unpredictable, delphinids will show larger home ranges and associate in larger bisexual schools for predator avoidance and cooperative foraging. This in turn may facilitate the formation of long-term social bonds between females if cooperation for offspring care is beneficial, but few long-term bonds between males are likely to form because males are unable to sequester individual females. It also predicts that because resource availability occurs in a range of complex distributions, in some circumstances, intermediate ranging patterns may emerge, where dolphins form medium-sized schools as a way of balancing intra-group competition for food and predation protection.

Delphinid life history traits

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

Delphinids are long-lived animals, with delayed maturity, low lifetime reproductive rates and high level of maternal investment, although considerable variation exists in these traits within the family (Table 2).

Table 2.   Summary of life history parameters in delphinids
SubfamilySpeciesLength (m)SSD (length)Longevity (years)Age at sexual maturity (years)Gestation (months)Age at weaning (years)IBI (years)
MFMF
  1. SSD, sexual size dimorphism; M, male; F, female; IBI, inter-birth interval.

  2. Southeastern Atlantic.

  3. Northeastern Pacific.

  4. §Gulf of Mexico.

  5. Eastern tropical Pacific (coastal).

  6. ††Southwestern Indian.

  7. ‡‡Northwestern Pacific.

  8. §§Northeastern Atlantic.

  9. †††Northwestern Atlantic.

LissodelphininaeCephalorhynchus commersonii1.301.340.97≥185–95–912  
Cephalorhynchus hectori1.461.630.90≥206–97–910–11 2–4
Cephalorhynchus heavisidii∼1.70        
Cephalorhynchus eutropia∼1.70   5–95–9   
Lagenorhynchus obscurus1.881.910.98 4–54–61212.5
Lagenorhynchus cruciger1.901.801.06      
Lagenorhynchus obliquidens1.901.920.99 108–1111  
Lissodelphis borealis2.632.171.21≥42101012 2
Lagenorhynchus australis2.202.101.05      
Lissodelphis peronii∼3.00        
 Sotalia guianensis1.701.870.9130–3575–812 2
Sotalia fluviatilis1.872.060.9830–35     
DelphininaeStenella longirostris1.92§1.89§1.02§207–104–7101–23
Stenella clymene1.971.901.04      
Stenella attenuata2.282.091.094612–159–1111.51.72.5–4
Stenella frontalis2.302.301.00 ?  8–15 ≤51–5
Stenella coeruleoalba2.35††2.18††1.08††≤587–155–1312–131.14
Lagenodelphis hosei2.362.351.00≥187–105–8   
Tursiops aduncus2.382.351.01 ≥12≥12122.6–5.33–6
Delphinus delphis2.42‡‡2.12‡‡1.14‡‡≥253–122–711.50.51–3
Delphinus capensis2.542.221.14      
Tursiops truncatus2612511.0440–509–145–13 1.5–23–6
Sousa chinensis2.802.601.08  9–10   
Sousa teuszii∼2.80        
 Lagenorhynchus acutus2.50§§2.24§§1.12§§≥226–126–12110.92.5
Steno bredanensis2.32§2.31§1.004§≥361410   
Lagenorhynchus albirostris2.60††2.59††1.003†† 131610  
Orcaella heinsohni∼2.70  ≥30     
Orcaella brevistoris∼2.75  ∼30  14  
GlobicephalinaePeponocephala electra2.682.601.03 16.511.5   
Feresa attenuata∼2.70        
Grampus griseus3.803.801.00≥35     
Globicephala macrorhynchus4.53‡‡3.58‡‡1.27‡‡≥6313–178–914.5–162–2.8 
Globicephala melas5.45†††3.81†††1.43†††35–45 (M) >60 (F)128123.7 
Pseudorca crassidens5.32§§4.47§§1.19§§57 (M) 62 (F)8–148–1415.51.8 
 Orcinus orca9.45§§5.66§§1.67§§50–60 (M) 80–90 (F)1510–1515–181–25

The smaller delphinids appear to live to just under 20 years of age, while medium-sized to larger delphinids can live for over 60 years (Table 2). In cetaceans, longevity is closely related to body size (Whitehead & Mann 2000). Delphinids range in length from about 1.3 to 1.8 m in the smallest species (e.g. genera Cephalorhyncus and Sotalia) to the large killer whales, which can reach lengths of almost 10 m (Table 2). There is also significant variation in sexual size dimorphism (SSD; Table 2), which is correlated with body size (Connor et al. 2000). Females attain slightly larger size than males in a few of the smaller delphinids, males attain slightly larger size than females in most of the small species, and greater male-biased SSD is seen in the larger delphinids (Table 2). Larger males also generally have larger propulsion structures and weapons, which are probably involved in male–male competition (Wells et al. 1999).

There are also differences in the age delphinids reach sexual maturity, with males and females reaching sexual maturity at a similar young age in Lissodelphininae and females generally maturing at a younger age than males in Delphininae and Globicephalinae (Table 2). Gestation, age at weaning and inter-birth interval also vary within delphinids (Table 2). Inter-birth interval generally increases with body size and correlates with gestational time and the duration of lactation (Whitehead & Mann 2000). Large delphinids of the genera Globicephala, Pesudorca and Orcinus show the lowest rates of prenatal growth (length at birth/gestation period) among cetaceans, suggesting very low prenatal energetic effort (Huang et al. 2011).

Additional information on reproductive parameters in delphinids, male reproductive strategies and female reproductive strategies and life histories in cetaceans is available in Perrin & Reilly (1984), Wells et al. (1999), Connor et al. (2000) and Whitehead & Mann (2000).

Dispersal patterns in delphinids and kin availability

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

Female philopatry is likely to be favoured when resources are spatially and temporally predictable, which in the case of delphinids is more likely to occur in inshore and coastal areas compared to pelagic environments. Recent genetic studies have demonstrated female-biased philopatry for several inshore and coastal populations of small delphinids (Table 3). In these philopatric populations, females have the potential to spend their lives in close association or spatial proximity with their maternal kin, thus creating opportunities for the development of kin-biased affiliations and behaviours (e.g. Möller et al. 2006; Frere et al. 2010b). In at least two Indo-Pacific bottlenose dolphin (T. aduncus) populations, males also show a moderate degree of philopatry (Krützen et al. 2004; Möller & Beheregaray 2004). Based on long-term behavioural data, Connor et al. (2000) suggested the possibility of locational bisexual philopatry for bottlenose dolphins, by which males would include their natal home range into their adult home ranges. The availability of male kin in these populations could then lead to the presence of male relatives in cooperative alliances (e.g. Krützen et al. 2003) and associations between male and female kin (e.g. Wiszniewski et al. 2010).

Table 3.   Dispersal tendencies in delphinid populations inferred based on genetic data
SpeciesOcean regionEnvironmentDispersal tendenciesStatistical testsNumber of samplesReferences
  1. FB, female-biased; MB, male-biased; BD, bisexual dispersal; BP, bisexual philopatry. FST, ΦST, fixation indices; mAIC, mean of corrected assignment index; vAIC, variance of corrected assignment index; r, relatedness; FIS, inbreeding coefficient.

  2. MB suggested based on higher values for female comparisons, although nonsignificant test results.

  3. MB suggested based on significant ΦST differences between males and females.

  4. §BD suggested but FIS significantly greater for females.

  5. BD suggested but significant FST differences between males and females for localities with small sample sizes.

Tursiops aduncusSouthwestern PacificInshoreMBmAIC, r54, 35Möller & Beheregaray (2004) and Möller et al. (2007)
Tursiops aduncusSoutheastern IndianInshoreMBFST, ΦST, Nm302Krützen et al. (2004)
Tursiops truncatusGulf of MexicoInshoreMBFST56Sellas et al. (2005)
Tursiops aduncusSouthwestern IndianCoastalMBmAIC, vAIC, FST142Natoli et al. (2008b)
Tursiops truncatusNorthwestern AtlanticPelagicMBmAIC, vAIC, r, FST, FIS404Rosel et al. (2009)
Tursiops sp.Southern IndianInshoreMBmAIC, r, FST50Bilgmann et al. (2007)
Stenella coerueloalbaMediterranean Sea and Northeastern AtlanticPelagicMBr165Gaspari et al. (2007)
Stenella frontalisNorthwestern Atlantic, including Gulf of MexicoCoastal and pelagicMBFST, ΦST199Adams & Rosel (2006)
Stenella longirostrisSouth Pacific OceanPelagic (inshore for resting)MBFST and ΦST, νAIc154Oremus et al. (2007)
Lagenorhynchus obscurusSoutheastern Pacific, Southwestern Atlantic, Southwestern PacificCoastal and pelagicMBvAIC, FST120Cassens et al. (2005)
Tursiops truncatusNorthwestern AtlanticCoastalBDFST58Parsons et al. (2006)
Tursiops truncatusGulf of MexicoCoastalBDFST185Sellas et al. (2005)
Tursiops truncatusMediterranean Sea, Black Sea and Northeastern AtlanticPelagicBDmAIC, vAIC, r, FST, FIS145Natoli et al. (2005)
Tursiops truncatusNorth AtlanticPelagicBDmAIC, vAIC, r, FST, FIS112Querouil et al. (2007)
Tursiops aduncusSouthwestern PacificCoastalBDmAIC, r, FST51, 131Möller et al. (2007) and Wiszniewski et al. (2010)
Tursiops sp.Southern IndianCoastalBDmAIC, r, FST34Bilgmann et al. (2007)
Delphinus delphisSouthern IndianCoastal and pelagicBDmAIC, r, FST72Bilgmann et al. (2009)
Delphinus delphisSouthwestern PacificPelagicBDmAIC, FST115Möller et al. (2011)
Delphinus delphisBlack Sea, Mediterranean Sea and Northeastern AtlanticPelagicBD§mAIC, vAIC, r, FST, FIS118Natoli et al. (2008a)
Delphinus delphisNorth AtlanticPelagicBDmAIC, vAIC, r, FST, FIS424Mirimin et al. (2009)
Delphinus delphisNortheast AtlanticPelagicBDFST150Querouil et al. (2010)
Delphinus delphisNortheastern Atlantic, Eastern Atlantic, Northwestern Atlantic, South AtlanticPelagicBDmAIC, FST, FIS156Natoli et al. (2006)
Delphinus capensisSouthwestern IndianPelagicBDmAIC, FST, FIS43Natoli et al. (2006)
Stenella attenuataEastern tropical PacificCoastal and pelagicBDFST225Escorza-Trevino et al. (2005)
Stenella frontalisNortheastern AtlanticPelagicBDFST193Querouil et al. (2010)
Stenella longirostrisNorth PacificPelagic (inshore for resting)BDmAIC, vAIC, r, FST, FIS505Andrews et al. (2010)
Lagenorhynchus acutusNorth AtlanticPelagicBDr42Mirimin et al. (2011)
Globicephala melasNorth AtlanticPelagicBPr193Amos et al. (1993)
Orcinus orcaNorth Atlantic and North PacificCoastal and pelagicBPr213Pilot et al. (2010)

By contrast, in pelagic waters where resources are likely to be less predictable, genetic analyses of several populations of small delphinids suggest that both males and females are likely to disperse, with no significant sex bias in dispersal (Table 3). Opportunities for association between kin in populations exhibiting bisexual dispersal, or among individuals of the dispersing sex, however, may still arise if there is dispersal of paternally related cohorts, if kin of different cohorts disperse together or if individuals disperse into groups already containing genetic relatives.

Evidence for an exception to the above-mentioned patterns comes from long-term behavioural studies and genetic data from killer whales (Orcinus orca) and long-finned pilot whales (Globicephala melas), where neither males nor females appear to disperse from their natal groups (Table 3). This is challenging to explain as the balance between benefits of kin cooperation and the costs of inbreeding is predicted to increase the magnitude of sex-biased dispersal with an increase in social complexity (Perrin & Goudet 2001). This unusual pattern among mammals, which was first demonstrated based on long-term behavioural data (Bigg et al. 1987, 1990), was recently genetically confirmed for several populations of killer whales from the North Pacific and North Atlantic (Pilot et al. 2010; Table 3). Connor (2000) suggested that the lower costs of locomotion for cetaceans in the aquatic environment could reduce the cost of philopatry for odontocetes compared to terrestrial mammals, as observed for the killer and pilot whales. The most extreme case is the fish-eating killer whales of British Columbia and Washington Strait. These killer whales are found in stable matrilineal groups, with no dispersal observed by either sex (Bigg et al. 1987, 1990). This dispersal pattern is in contrast to the sympatric marine mammal-eating killer whale, despite extensive geographic overlap. Mammal-eating whales are generally found in smaller groups and appear to be composed of only a single matriline with up to two generations. From these groups, females may disperse when their first calf is born, or males, other than the firstborn, before sexual maturity (Baird 1994; Baird & Dill 1995; Baird 2000). Smaller groups appear to be optimal for foraging their main prey, harbour seals (Baird & Dill 1995), suggesting that dispersal in these animals is related to foraging efficiency. Long-finned pilot whales also appear to display a pattern of bisexual philopatry, with molecular typing revealing that large pods of pilot whales caught in a drive fishery consisted of single extended families (Amos et al. 1991, 1993). Differences in philopatric and dispersal patterns impact on the kinship structure of groups and in turn will affect social relationships among individuals (Clutton-Brock & Lucas 2011). Therefore, among the delphinids, the prospects for association and potentially cooperation with a large number of relatives appear to be highest among these bisexually philopatric toothed whales.

Genetic relatedness, kin associations and mating patterns in delphinids

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

Analysis of relatedness and parentage in delphinids is still in its infancy (Table 4). Kinship relationships in delphinid schools are best known from studies of bottlenose dolphins living in inshore environments, where strong female philopatry and moderate male philopatry were suggested (Möller & Beheregaray 2004; Krützen et al. 2004). Genetic studies in populations of Indo-Pacific bottlenose dolphins from Australia suggested that females form moderate social bonds with maternally and biparentally related females (Möller et al. 2006; Frere et al. 2010b; Table 4) but also associate closely with unrelated females, including those in similar reproductive status (Möller & Harcourt 2008). In addition, certain females in one population associated closely with related adult males (Wiszniewski et al. 2010; Table 4). Altogether, these results imply kin recognition in delphinids (Box 1).

Table 4.   Patterns of genetic relatedness within delphinid groups
SpeciesAreaDispersal tendenciesRelatedness patternsSample typeNumber of samplesReference
  1. MB, male-biased; BD, bisexual dispersal; BP, bisexual philopatry; m, males; f, females.

  2. Mass stranding.

  3. Single strandings.

  4. §Biopsies from captive and free-ranging animals.

Tursiops sp.Shark Bay, Western AustraliaMBFirst-order and second-order allied males are more related than expected by chance; superallied males are randomly relatedBiopsies162 mKrützen et al. (2003)
Females associate preferentially with maternal and biparentally related femalesBiopsies46 fFrere et al. (2010b)
Tursiops truncatusSarasota Bay, FloridaMBFemales associate with maternal kin within bandsBlood samples60Duffield & Wells (1991)
Allied males are randomly relatedBlood samples81 mOwen (2003)
Tursiops aduncusPort Stephens, eastern AustraliaMBAssociated and allied males are randomly relatedBiopsies20 mMöller et al. (2001)
Females associate preferentially with maternally related femalesBiopsies21 fMöller et al. (2006)
Females associate preferentially with genetic related females and malesBiopsies25 f, 29 mWiszniewski et al. (2010)
Tursiops truncatusLittle Bahamas BankBDAllied males are more related than expected by chanceBiopsies, faecal samples21 mParsons et al. (2003)
Stenella coeruleoalbaLigurian SeaMBAssociated females in small groups are more related than expected by chance; associated males are randomly relatedBiopsies and scrub pads33 f, 29 mGaspari et al. (2007)
Delphinus delphisBay of Biscay and English Channel Average relatedness within pods not significantly different than average relatedness between pods, but large mass stranding likely to include half sibshipsStrandings51 f, 1 m; 24 f, 18 mViricel et al. (2008)
Lagenorhynchus acutusWest IrelandBDGroups consisted of multiple maternal lineages, mostly unrelated adults and mother-offspring calvesStrandings15 f, 21 mMirimin et al. (2011)
Orcinus orcaWashington State, southeast Alaska, Kamchatka Russia, Aleutians and Bering Sea, North Pacific offshore, California, southeast IcelandBPAverage relatedness within pods was significantly higher than average relatedness within populations, but lower in ‘transient’ compared to ‘resident’ ecotypes; average relatedness of females higher than males in Washington State and Alaskan resident populations and the reverse pattern in transient, offshore and Russian resident populationsStrandings, biopsies§87 f, 126 mPilot et al. (2010)
Globicephala melasFaroe Islands, North AtlanticBPPod members were from a single extended familyDrive fishery193Amos et al. (1991)
Table Box 1.   Potential mechanisms of kin recognition in delphinids
Kin recognition is the ability to distinguish between individuals of different degrees of genetic relatedness (Hepper 1991). In delphinids, kin recognition is likely to occur via social familiarity. In bottlenose dolphins, juveniles usually remain loosely associated with their mothers, but associate more closely with them when their siblings are born (Wells 1991). Therefore, young dolphins have opportunities to become familiar with at least maternal siblings of adjacent cohorts. Female bottlenose dolphins have also been observed to return to their natal band when their fist calves were born (Wells 1991) and continued to associate with their mothers after conceiving calves (Smolker et al. 1992), suggesting that mother–daughter social bonds continue into adulthood. Another mechanism for individual and possibly kin recognition is through vocal communication. Dolphins produce a large array of vocalizations, and among these are individually distinctive whistles, called signature whistles (Caldwell & Caldwell 1965; Caldwell et al. 1990). In bottlenose dolphins, there is strong evidence that these sounds play a role in individual recognition, including that of close kin (Sayigh et al. 1999; Janik et al. 2006). Playback experiments have shown that bottlenose dolphins respond more strongly to whistles of closely related than to those of unrelated but familiar individuals (Sayigh et al. 1999). This has been also demonstrated in a similar experiment but using synthetic whistles from which all voice features were removed, suggesting that signature whistles may be used as referential signals similar to the use of names in humans (Janik et al. 2006). Signature whistles are also used for maintaining group cohesion (Janik & Slater 1998), including that between kin (Smolker et al. 1993). In captivity, dolphins were more likely to produce signature whistles when one of the group members voluntarily swam to a different pool (Janik & Slater 1998). In the wild bottlenose dolphin, calves whistled more often towards the end of mother–calf separations, just before reunions (Smolker et al. 1993). Allied male bottlenose dolphins also converge to similar whistles as social bonds strengthen (Watwood et al. 2004). While most studies on the function of signature whistles have been conducted in bottlenose dolphins, these whistles have also been reported in several other dolphin species, including short-beaked common dolphins (Caldwell & Caldwell 1968), Pacific white-sided dolphins (Caldwell & Caldwell 1971), Atlantic spotted dolphins (Caldwell & Caldwell 1973) and humpback dolphins (Van Parijs & Corkeron 2001). Killer whales that live in highly stable matrilineal pods (Bigg et al. 1990) are known to have distinctive group-specific vocal repertoires (Riesch et al. 2006). Call structure is known to reflect both maternal relatedness and social affiliation, providing a mechanism for kin recognition, and also to facilitate social decisions (Deecke et al. 2010). Moreover, individuals within groups produce calls with different frequency contours, suggesting that these whales may also be able to distinguish between the highly similar shared calls of their matrilineal relatives (Nousek et al. 2006).

Male bottlenose dolphins in some inshore populations associate strongly with other males forming alliances and coalitions that cooperate to gain access to receptive females for mating (Wells et al. 1987; Connor et al. 1992, 1999; Möller et al. 2001; Wiszniewski et al. accepted; Tables 4 and 5). Strong male bonds and the formation of coalitions have also been suggested for other members of the subfamily Delphininae (Atlantic spotted dolphins, S. frontalis, Herzing & Johnson 1997; spinner dolphins, S. longirostris, Norris & Johnson 1994). In bottlenose dolphins, male alliance formation has been documented in populations with male-biased and female-biased dispersal patterns (Table 5), and therefore, this cooperative behaviour appears to have evolved independently of dispersal tendencies. Members of stable alliances are closely related in some populations (Krützen et al. 2003; Parsons et al. 2003; Tables 4 and 5), but in other populations, allied males are on average only randomly related (Möller et al. 2001; Owen 2003; Wiszniewski et al. in press; Tables 4 and 5). In one population where males in stable alliances were on average more related than expected by chance (Krützen et al. 2003), the reproductive success of males within some of the alliances was significantly skewed (Krützen et al. 2004). Levels of inbreeding in this population were higher than expected by chance, with young, less experienced mothers producing earlier calves that are more inbred and less fit (Frere et al. 2010a). By contrast, in a population where allied males are on average randomly related, reproductive skew within alliances was not significantly different from random expectations, although there was a moderate degree of polygyny in the population with males in larger alliances fathering more calves per capita (Wiszniewski et al. 2011). In another species, the Atlantic spotted dolphin, age appears to have an effect on male reproductive success (Green et al. 2011).

Table 5.   Male alliance formation in populations of bottlenose dolphins (genus Tursiops) with available genetic data
SpeciesPopulationAlliance typeAlliance sizeRelatednessDispersalSex ratioSSD (length)IBI (years)References
  1. MB, male-biased; BD, bisexual dispersal; SSD, sexual size dimorphism (body length); IBI, inter-birth interval.

  2. Estimated based on the proportion of biopsy sampled adult males and females.

  3. Estimated based on 2 adult males and 2 adult females reported in Smolker et al. (1992).

  4. §Based on capture-released animals.

  5. Estimated based on measures from eastern Australian T. aduncus reported in Hale et al. (2000).

  6. ††Möller (unpublished data).

Tursiops sp.Shark BayFirst order2–3Greater than expected by chanceMB0.81.0043–6Smolker et al. (1992), Mann et al. (2000) and Krützen et al. (2003, 2004)
Tursiops sp.Shark BaySecond order5–6Greater than expected by chanceMB0.81.0043–6Smolker et al. (1992) and Krützen et al. (2003, 2004)
Tursiops sp.Shark BaySuperalliance14Randomly relatedMB0.81.0043–6Smolker et al. (1992) and Krützen et al. (2003, 2004)
Tursiops truncatusSarasota BayFirst order2Randomly relatedMB0.7§1.0603–6Wells et al. (1987), Wells (1991), Scott et al. (1990) and Tolley et al. (1995)
Tursiops aduncusPort StephensFirst order2–4Randomly relatedMB0.81.0033–5††Möller et al. (2001) and Wiszniewski et al. (2009)
Tursiops truncatusBahamasFirst order2Greater than expected by chanceBD0.9  Parsons et al. (2006)

Information on the degree of genetic relatedness of delphinid schools living in coastal and pelagic waters, where bisexual dispersal is typical, is scarcer. In the striped dolphin, analysis of genetic relatedness showed higher average relatedness between adult females within small schools, suggesting that females preferentially associate with adult kin in these groups (Gaspari et al. 2007; Table 4). In some other dolphin species living in open environments and usually found in large schools, genetic relatedness has been investigated based on samples from stranded animals. Short-beaked common dolphins, for example, do not appear to associate preferentially with relatives, but sex, age and sexual maturity may influence associations in these animals (Viricel et al. 2008; Table 4). A similar pattern is also suggested for Atlantic white-sided dolphins where groups were mainly composed of unrelated adult individuals and calves, with juveniles absent from the groups studied (Mirimin et al. 2011; Table 4). Calves in the latter study were not closely related to each other, suggesting that the mating system was more likely to be promiscuous (Mirimin et al. 2011). Large group sizes and promiscuous mating systems, coupled with the bisexual dispersal patterns of pelagic dolphins, should lead to dilution of genetic relatedness values within schools (e.g. Lukas et al. 2005; Holekamp et al. 2011). By contrast, genetic analyses of several populations of killer whales in the North Pacific and North Atlantic demonstrated very high levels of genetic relatedness within pods, both within and between sexes (Pilot et al. 2010; Table 4). In these animals, gene flow appears to be mainly mediated by males during temporary associations of pods and temporary dispersal of males between pods, populations and ecotypes, with only a few cases of permanent dispersal genetically suggested (Pilot et al. 2010; Foote et al. 2011; Ford et al. 2011). As in the closed societies of bats, maternally inherited mtDNA should be highly conserved among group members, while biparentally inherited nuclear DNA should be less structured depending on the level of gene flow (Kerth & Van Schaik 2011). Recent paternity analyses in these animals revealed contrasting male reproductive behaviours, with low skew and half of the paternities assigned to males from different populations in one study (Pilot et al. 2010) and moderate skew and most matings occurring within pods in another (Ford et al. 2011).

Towards a comprehensive framework for the evolution of delphinid social systems

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

Predictability of resources and dispersal patterns: female bonding in small delphinids

In this review I showed that in small delphinids, female-biased philopatry is primarily observed in populations residing in inshore waters (Table 3), where predictable resources are more likely to be found compared to other marine environments (e.g. Wells et al. 1999; Gowans et al. 2008). Female philopatry in these areas is likely to occur because of differences in PRR of male and females, and females benefiting more than males from familiarity with food resources. Genetic studies further indicated that these females preferentially associated with female kin (Table 4). In addition, results from behavioural studies suggested that they also associate closely with other females in similar reproductive states (Wells et al. 1987; Möller & Harcourt 2008). Thus, under these circumstances, I propose that moderate female social bonds emerge between kin and nonkin, although long-term social bonds may preferentially occur between female kin. This conflicts with the prediction of loose social networks of females based on reproductive status, which was proposed by Gowans et al. (2008). Benefits for the formation of these bonds include calf protection from predators, male harassment and possibly infanticide, the latter two depending on the degree of sexual conflict between males and females, which relates to the bias in the OSR.

By contrast, the majority of genetic studies of small delphinids inhabiting coastal and pelagic environments revealed bisexual dispersal tendencies (Table 1). In these areas, dolphins generally exhibit large home ranges because of the unpredictability of food resources (Wells et al. 1999; Gowans et al. 2008). Therefore, in these environments, there may be no food-related advantages for females to remain philopatric, and both females and males will tend to disperse. Females may still associate preferentially with females in similar reproductive condition. Thus, under these circumstances, I predict that female associations and weak bonds occur irrespective of kinship. This also disagrees with the socio-ecological model, which suggested the formation of long-term social bonds between females if cooperation for offspring care was beneficial (Gowans et al. 2008). However, if there is between-group competition for critical resources (e.g. resting refuge for spinner dolphins in remote atolls; Karczmarski et al. 2005), geographic isolation (e.g. common bottlenose dolphins in Doubtful Sound, New Zealand; Lusseau et al. 2003) or sexual conflict, moderate to strong social bonds may emerge.

Life history and sexual conflict: male bonding in small delphinids

Here I showed that the formation of male bonding appears restricted to the Delphininae, in species with small male-biased sexual size dimorphism and moderate inter-birth interval, and occurs independently of dispersal tendencies (Tables 1 and 5). I suggest that male alliance formation is a mechanism for increasing the power of males for coercing females for mating and for male–male competition. Different relatedness patterns in alliances of bottlenose dolphins (Table 5), and no alliance formation in some populations, support the existence of different male mating strategies within and between populations. Although nonkinship-related factors are probably involved in the choice of alliance partners (Möller et al. 2001), when related males are present within an alliance, kin selection may operate (Krützen et al. 2004). Thus, I propose that the formation of male social bonds as alliances or coalitions occurs independent of dispersal tendencies and kinship and will develop in species with small male-biased SSD and male-biased OSR. In the socio-ecological model, long-term bonds between males for sequestering individual females for mating were only proposed for males inhabiting inshore environments, where females generally associate in small groups. I further suggest that although promiscuity seems the most plausible mating system for small delphinids, the formation of male alliances may lead to a mating system characterized by moderate polygyny.

Life history and sexual conflict: bisexual kin bonding in large delphinids

I reviewed evidence for the unusual pattern of bisexual philopatry in large delphinids and the occurrence of matrilineal societies (Tables 1 and 3). Large body size appears to have evolved twice in the delphinid lineage (e.g. McGowen 2011), and this is also the case for matrilineal social structures, because it is represented in members of the subfamily Globicephalinae and in the genus Orcinus. Whales of these societies generally range over large distances because of the unpredictability of their food resources (e.g. Baird 2000), and therefore, bisexual kin bonds are unlikely to have arisen because of strong resource competition. However, kin bonds may facilitate cooperative foraging, food sharing and social learning of foraging techniques (e.g. Guinet 1991; Hoelzel 1991, 1993). Cultural transmission of foraging specializations and vocal sounds has been proposed for killer whales and bottlenose dolphins, but occurs both inside and outside the immediate kin group (e.g. Guinet 1991; Deecke et al. 2010; Watwood et al. 2004; Krützen et al. 2005; Sargeant et al. 2005).

I suggest that matrilineal societies in large delphinids have primarily evolved for protection of calves and females from potential male harassment and injuries. Bonds in turn may have facilitated the evolution of kin-biased behaviours. Females in these species show long gestation and lactation, probably leading to a male-biased OSR. In addition, there is a high potential risk of injury from males because of the high SSD between males and females. Although male coercion of females and calves, and male–male competition, appears to be a rare event, the formation of matrilineal societies may be a successful strategy that led to low prospective for effectiveness in male coercion. In at least one killer whale population, units with large number of adult males rarely associate with other units, which could be related to the costs of foraging in larger groups (Ivkovich et al. 2009) or could represent avoidance by other units.

The formation of mother–sons bonds in these animals, although more difficult to explain, could also relate to protection of females and their calves, and this being best attained by the presence of protector male(s) because of the high SSD between females and males. Males on the other hand could benefit through inclusive fitness gains, and also from knowledge transfer of habitat and the location of food resources, particularly from the matriarch. In turn, ‘good sons’ could be preferentially chosen as mates by females. In killer whales, where some feeding specializations favour small groups (e.g. Baird 2000), matriarchs may prefer the primogenitor to remain philopatric because of preferential investment on the offspring with higher potential of reproductive output. Recent genetic studies on these animals showed that male reproductive success appears to increase with age and body size (Ford et al. 2011), and males do not breed with female kin (Pilot et al. 2010; Ford et al. 2011), suggesting the evolution of a mechanism for inbreeding avoidance in philopatry (see Box 1).

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

Ecological factors, particularly food distribution and predation risk, have been proposed as the main driving forces of delphinid sociality. Here, I showed that environment type, which relates to food predictability and delphinid ranging patterns, impacts upon dispersal tendencies, with small delphinids that live in fission–fusion societies generally exhibiting female-biased philopatry in inshore waters and bisexual dispersal in coastal and pelagic waters. When female philopatry occurs, females preferentially associate with kin and form moderate social bonds with them. Male bonding occurs in species of Delphininae with small male-biased SSD and male-biased OSR, and this behaviour is independent of dispersal tendencies. Males form alliances preferentially with genetically related males or irrespective of kinship, and this has an effect on reproductive skew within alliances.

By contrast, large delphinids, which live in coastal and pelagic waters, show bisexual philopatry and live in matrilineal societies (Orcinus, and possibly Globicephala and Pseudorca). Risk of predation and food competition are unlikely to explain these bisexual kin bonds. It is proposed that protection of calves and females because of sexual conflict may have favoured the formation of these societies. In turn, kin bonds facilitated the evolution of kin-biased behaviours.

Only a few paternity studies have been conducted for delphinids so far, and these, combined with information of large testes relative to their body mass (Connor et al. 2000), point towards promiscuity and moderate polygyny as the most plausible mating systems. Studies on populations of the same species inhabiting disparate environments, and studies of less related species living in similar habitats, would contribute towards unravelling ecological and intrinsic factors shaping the evolution of delphinid social systems. Preferably, these studies would combine long-term behavioural observations, genetic information on relatedness and parentage, life history and demographic data towards building a comprehensive framework for the evolution of delphinid social systems.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References

I would like to thank Joanna Wiszniewski, Guido Parra, Luciano Beheregaray and two anonymous reviewers for comments and suggestions to the manuscript; Katharina Peters for assistance with tables and referencing; and Bernd Würsig and Randall Wells for their inspiration to researching dolphin social systems.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. The social structure of delphinids
  5. The delphinid socio-ecological model
  6. Delphinid life history traits
  7. Dispersal patterns in delphinids and kin availability
  8. Genetic relatedness, kin associations and mating patterns in delphinids
  9. Towards a comprehensive framework for the evolution of delphinid social systems
  10. Conclusions
  11. Acknowledgements
  12. References
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L.M. is a behavioural and molecular ecologist interested in the evolution of mammalian social systems and the conservation management of whales and dolphins. She heads the Cetacean Ecology, Behaviour and Evolution Lab at Flinders University of South Australia.