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The Phylogenetic Roots of Human Lethal Violence José María Gómez1,2, Miguel Verdú3, Adela González-Megías4 & Marcos Méndez5

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The Phylogenetic Roots of Human Lethal Violence José María Gómez1,2, Miguel Verdú3, Adela González-Megías4 & Marcos Méndez5 LETTER doi:10.1038/nature19758 The phylogenetic roots of human lethal violence José María Gómez1,2, Miguel Verdú3, Adela González-Megías4 & Marcos Méndez5 The psychological, sociological and evolutionary roots of 600 human populations, ranging from the Palaeolithic era to the present conspecific violence in humans are still debated, despite attracting (Supplementary Information section 9c). The level of lethal violence the attention of intellectuals for over two millennia1–11. Here we was defined as the probability of dying from intraspecific violence propose a conceptual approach towards understanding these roots compared to all other causes. More specifically, we calculated the level based on the assumption that aggression in mammals, including of lethal violence as the percentage, with respect to all documented humans, has a significant phylogenetic component. By compiling sources of mortality, of total deaths due to conspecifics (these sources of mortality from a comprehensive sample of mammals, were infanticide, cannibalism, inter-group aggression and any other we assessed the percentage of deaths due to conspecifics and, type of intraspecific killings in non-human mammals; war, homicide, using phylogenetic comparative tools, predicted this value for infanticide, execution, and any other kind of intentional conspecific humans. The proportion of human deaths phylogenetically killing in humans). predicted to be caused by interpersonal violence stood at 2%. Lethal violence is reported for almost 40% of the studied mammal This value was similar to the one phylogenetically inferred for species (Supplementary Information section 9a). This is probably the evolutionary ancestor of primates and apes, indicating that a an underestimation, because information is not available for many certain level of lethal violence arises owing to our position within species. Overall, including species with and without lethal violence, the phylogeny of mammals. It was also similar to the percentage we found that the percentage of deaths due to conspecifics was seen in prehistoric bands and tribes, indicating that we were as 0.30 ±​ 0.19% of all deaths (phylogenetically corrected mean ± s.e.m). lethally violent then as common mammalian evolutionary history This level was not affected by the number of individuals sampled would predict. However, the level of lethal violence has changed per species (Supplementary Information section 1). These findings through human history and can be associated with changes in suggest that lethal violence, although infrequent, is widespread among the socio-political organization of human populations. Our study mammals19–21. provides a detailed phylogenetic and historical context against We determined whether related species tended to have similar levels which to compare levels of lethal violence observed throughout of lethal violence by calculating the phylogenetic signal. We used the our history. most recently updated mammalian phylogenies, including 5,020 Debate on the nature of human violence has been ongoing since extant mammals22 and 5,747 extant and recently extinct mammals 23. before the publication of Leviathan by Thomas Hobbes in 1651. We found a significant phylogenetic signal for lethal violence, even Lethal violence is considered by some to be mostly a cultural trait5,6,12; after combining disparate causes of intraspecific killings (λ > 0.60, however, aggression in mammals, including humans13,14, also has a P <​ 0.0001; Supplementary Information section 2). While lethal genetic component with high heritability. Consequently, it is widely violence was uncommon in certain clades such as bats, whales and acknowledged that evolution has also shaped human violence2–4. lagomorphs, it was frequent in others, such as primates (Fig. 1). The From this perspective, violence can be seen as an adaptive strategy, phylogenetic signal was also significantly lower than one (P <​ 0.0001), favouring the perpetrator’s reproductive success in terms of mates, indicating that lethal violence exhibits certain evolutionary flex- status or resources15,16. Yet this does not mean that violence is invariant ibility (Fig. 1). For example, the level of lethal violence strongly or even adaptive in all situations15. In fact, given that the conditions differs between chimpanzees (Pan troglodytes) and bonobos under which violence benefits evolutionary fitness depend on the (Pan paniscus)10,17,20. This outcome suggests that additional factors ecological and cultural context, levels of violence tend to vary among may subsequently modify the level of lethal violence in related species. human populations12,13,15,16. Disentangling the relative importance Territoriality and social behaviour mediate conspecific aggression in of cultural and non-cultural components of human violence is mammals20,24. We scored these two traits for every mammal in our challenging3,5 owing to the complex interactions between ecological, study and statistically related them to the level of lethal violence using social, behavioural and genetic factors. phylogenetic generalized linear models. Using this method, we found Conspecific violence is not exclusive to humans. Many primates that the level of lethal violence was higher in social and territorial exhibit high levels of intergroup aggression and infanticide4,10. Social species than in solitary and non- territorial species (Fig. 2; Extended carnivores sometimes kill members of other groups and commit Data Table 1). infanticide when supplanting older members of the same group17,18. The occurrence of a phylogenetic signal for lethal violence in Even seemingly peaceful mammals such as hamsters and horses mammals enables the phylogenetic inference of lethal violence in sometimes kill individuals of their own species19,20. The prevalence humans. We used ancestral-state estimation methods that infer the of aggression throughout Mammalia raises the question of the extent value of a trait in any extant species according to its position in the to which levels of lethal violence observed in humans are as expected, phylogenetic tree25. The level of human lethal violence was estimated given our position in the phylogenetic tree of mammals. In this study, both with and without considering the territoriality and sociability of we quantified the level of lethal violence in 1,024 mammalian species mammals. Because phylogenetic inferences are much more accurate from 137 families (Supplementary Information section 9a) and in over and reliable when including information from close relatives26 1Estación Experimental de Zonas Áridas (EEZA-CSIC), E-04120 Almería, Spain. 2Dpto de Ecología, Universidad de Granada, E-18071 Granada, Spain. 3Centro de Investigaciones sobre Desertificación (CSIC-UV-GV), E-46113 Valencia, Spain. 4Dpto de Zoología, Universidad de Granada, E-18071 Granada, Spain. 5Área de Biodiversidad y Conservación, Universidad Rey Juan Carlos, E-28933 Madrid, Spain. 13 OCTOBER 2016 | VOL 538 | NATURE | 233 © 2016 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. RESEARCH LETTER s E m u P i c u o i s M Fu i i e s P s s g E u s F n h Glau P t t i s e y a u l a e i u u C s c l una n a S o Ta s e a B i i t i u d s n scar M u l t d p s a i g r i a u al s s s a c t a s e r u e ra P i s r u a n e o d mb u e n S c S i mi en r u n Sy S u e i c E P n i t b g l u s n S s c u s t e u t l i c t o u m o o g s s gi e i c Gr e i y E r n c a e D un e a M li a o a o r u to e t u n s i n a om r c s i i t y s m h d r n f s n l d op a r a S lv hy etes u i n n s o s ni l r l u r i g s bu t p u g ry u i a n v S i Ra i e s ci s u e i o a s h a e r l u u yo a u om s a i t ma u o nus R ic o yl m s r d s i e y t o din i nu o i c n m i v p l r r m t a u la s r n y i c te l h s m n i u u i i l i n w u e o d l x s u r us l s p o i r r v s s u a u i i a u m s y u s i ag r a at l e s yth ia vi h l r g l l u i y r c us u a c a o x r h tu s r e m s n o us g s e Sylvi vi r r d u s g h p h o my ru s d l g s ic v t s y i p a e c s mc b r t k i b i a t t Le ys s i a s n c e r L f u s e s L l e r be u i u l g u o t u l n i e n us i s e a d ag i s ir c s i u v c a ulv e i i i p i la us n Pr l a g n u im f c y py a v r s a m l e a i u a p u p e s y u a a f s l fa a e e m er b g t r i i c s s c u c pe r r m d r a d s a ru u m unni s ni a u lu u h r p u n a pu n v s ib e s be p gu n p s s i v r s s p que s s u s u i l r r um c o r w o b s i e m t us s qu l u u l e i r Le i a u l L br b b l g f c e e o s r dm e u us i la i ella u i u m e u u st c e l g u u c u le s il t i a s i r s s s no s a d o r a ri Lepu L ra us h x s s i l r L r s nna n r s o v ep r r i s la ic i s r l r s lus r ys O u h i us s i e t s x s n s s a s s mu a e s a g as a l u r a ep a a in s y h t o e i o a s ep p aru u t ll u c G di u i ph i l u p u u i u u u a Lepus s f i h a i u n t p n i a o s at s i a y i l r n e olor r i i u s und u n r ca n m hi l av u m ph a p s low t r r a h a u i i m ore s u p i l t a u u L n r ia my o h o orid i t i yc ci u l u c c i lu e et i c m P s si l o p Le c c h x du ca s u P u m i s s a a a i m s s o oe n e e e u a i s m o h u s l us s o gus s e l nt u a r o m c s ari mi p v s s e a s i m o o l a ya ro ie S m S S m li nus r am a omys l m p S r S r ti h m op lus l di T s s s z i T a n p u b n pu s X X o t nut g a n i a L u u P P r o on e i m h l L p t f a n mo ph vi a o i ii i H a rmo o ic o n l T i er a t C n n T r p hi l o o gu T y m o a rm us Oc n L us a i r s e arcticu s s T hi r k a g eu rica a i m p ep us T yn o a on la r i T e
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