Genetic influences on social attention in free-ranging rhesus macaques

Abstract

An ethological approach to attention predicts that organisms orient preferentially to valuable sources of information in the environment. For many gregarious species, orienting to other individuals provides valuable social information but competes with food acquisition, water consumption and predator avoidance. Individual variation in vigilance behaviour in humans spans a continuum from inattentive to pathological levels of interest in others. To assess the comparative biology of this behavioural variation, we probed vigilance rates in free-ranging macaques during water drinking, a behaviour incompatible with the gaze and postural demands of vigilance. Males were significantly more vigilant than females. Moreover, vigilance showed a clear genetic component, with an estimated heritability of 12%. Monkeys carrying a relatively infrequent ‘long’ allele of TPH2, a regulatory gene that influences serotonin production in the brain, were significantly less vigilant compared to monkeys that did not carry the allele. These findings resonate with the hypothesis that the serotonin pathway regulates vigilance in primates and by extension provoke the idea that individual variation in vigilance and its underlying biology may be adaptive rather than pathological.

What have we been looking at? A call for consistency in studies of primate vigilance

“…Vigilance decreases with increasing neighbors Busia et al (2016), Cowlishaw (1998), Gaynor & Cords (2012) i , Rose & Fedigan (1995), Stojan-Dolar & Heymann (2010), Teichroeb & Sicotte (2012) Vigilance lower with at least one adult neighbor Steenbeek et al (1999), Stojan-Dolar & Heymann (2010), Treves (1998), Treves et al (2001), van Schaik & van Noordwijk (1989 Vigilance increases with increasing neighbors Kutsukake (2006Kutsukake ( , 2007 No significant effect Kutsukake (2006), Watson et al (2015) Distance to neighbors Vigilance increased as distance to nearest group member decreased Suzuki & Sigiura (2011) Vigilance increased as distance to nearest conspecific or heterospecific neighbor increased Robinson (1981), Stojan-Dolar & Heymann (2010) Vigilance higher with few neighbors near and many neighbors farther away, and vice versa.…”

“…Mothers with dependent infants more vigilant than those with independent young or females without infants Boinski et al (2003), Treves (1999c), Treves et al (2003) No difference found between adult females with or without infants Treves (1998) All adult individuals increased vigilance after birth of infants Treves et al (2001) Vigilance increased when infant-carrying Steenbeek et al (1999), Stojan-Dolar & Heymann (2010) Age Vigilance increases with age in both sexes Boinski et al (2003), Busia et al (2016), de Ruiter (1986, Fragaszy (1990), Gosselin-Ildari & Koenig (2012) Vigilance decreased with age in both sexes Watson et al (2015) No age-related effects Caine & Marra (1988) Activity Vigilance higher during resting and traveling van Schaik & van Noordwijk (1989) Vigilance higher during resting Cowlishaw (1998), Gaynor & Cords (2012), Stojan-Dolar & Heymann (2010), Suzuki & Sigiura (2011) Vigilance lower during grooming than resting or feeding Cords (1995) Routine vigilance higher during feeding Teichroeb & Sicotte (2012) No difference between feeding or resting Macintosh & Sicotte (2009), Teichroeb & Sicotte (2012 Vigilance higher during foraging than resting Kutsukake (2006) Isbell & Young (1993), Kazahari & Agetsuma (2010) f , Hill & Cowlishaw (2002) h Subgroup size Vigilance lower with larger subgroup sizes but only in boundary areas Busia et al (2016) No effect of daily party size Kutsukake (2006) Group composition…”

“…Despite both Kutsukake (2006) and Watson et al (2015) reporting that number of neighbors did not significantly affect vigilance in chimpanzees and rhesus macaques (Macaca mulatta) respectively, a host of other studies have shown vigilance use to decrease with increasing number of neighbors (Busia, Schaffner, & Aureli, 2016;Cowlishaw, 1998;Stojan-Dolar & Heymann, 2010), although sometimes only for specific behaviors (Stojan-Dolar & Heymann, 2010;Teichroeb & Sicotte, 2012). Robinson (1981) found that wedge-capped capuchins (Cebus olivaceus) increased vigilance with increasing distance to nearest neighbor; conversely, Suzuki and Sugiura (2011) reported vigilance increased as distance to nearest group member decreased in Japanese macaque (Macaca fuscata) adult females.…”

“…Robinson (1981) found that wedge-capped capuchins (Cebus olivaceus) increased vigilance with increasing distance to nearest neighbor; conversely, Suzuki and Sugiura (2011) reported vigilance increased as distance to nearest group member decreased in Japanese macaque (Macaca fuscata) adult females. Baldellou & Henzi (1992), Busia et al (2016), de Ruiter (1986, Fragaszy (1990), Gould et al (1997), Isbell & Young (1993), Rose & Fedigan (1995), Steenbeek et al (1999), Stojan-Dolar & Heymann (2010) a , Treves (1998Treves ( , 1999c, van Schaik & van Noordwijk (1989), Watson et al (2015) No difference between sexes Cowlishaw (1998), Gould (1996), Gould et al (1997), Macintosh & Sicotte (2009), Smith, Kelez & Buchanan-Smith (2004, Teichroeb & Sicotte (2012), Treves (1998) Dominance Subordinates more vigilant than dominants Alberts (1994) b , Caine & Marra (1988), Gaynor & Cords (2012), Haude et al (1976), Keverne et al (1978), Pannozzo et al (2007) High-ranking individuals more vigilant Alberts (1994) c , Gould (1996), Gould et al (1997), Isbell & Young (1993), Rose & Fedigan (1995), Watson et al (2015) No effect of rank Robinson (1981) Adult females with Infants…”

“…For example, vigilance increased in adult female blue monkeys when either of the two highest-ranking females were nearby (Gaynor & Cords, 2012), when individual mountain gorilla (Gorilla gorilla beringei) who share agonistic relationships were in proximity (Watts, 1998), and when non-affiliates were in proximity (Kutsukake, 2006). Vigilance in ursine colobus (Colo- Factors relating to focal animals, such as their age-sex class and dominance status also influence vigilance patterns (Chance, 1967), with numerous studies reporting males to be more vigilant than other agesex classes (Baldellou & Henzi, 1992;de Ruiter, 1986;Fragaszy, 1990;Gould, Fedigan, & Rose, 1997;Isbell & Young, 1993;Rose & Fedigan, 1995;Steenbeek et al, 1999;Treves, 1998Treves, , 1999cvan Schaik & van Noordwijk, 1989;Watson et al, 2015). Nevertheless, a number of other studies report no difference between sexes (Cowlishaw, 1998;Gould, 1996;Gould et al, 1997;MacIntosh & Sicotte, 2009;Teichroeb & Sicotte, 2012;Treves, 1998).…”