1. Evolutionary Biology
  2. Neuroscience

The evolution and biological correlates of hand preferences in anthropoid primates

  1. Kai R Caspar  Is a corresponding author
  2. Fabian Pallasdies
  3. Larissa Mader
  4. Heitor Sartorelli
  5. Sabine Begall
  1. Department of General Zoology, University of Duisburg-Essen, Germany
  2. Department of Game Management and Wildlife Biology, Faculty of Forestry and Wood Sciences, Czech University of Life Sciences, Czech Republic
  3. Institute for Theoretical Biology, Department of Biology, Humboldt-Universität zu Berlin, Germany
  4. Independent researcher, Brazil
https://doi.org/10.7554/eLife.77875
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Cite this article
  1. Kai R Caspar
  2. Fabian Pallasdies
  3. Larissa Mader
  4. Heitor Sartorelli
  5. Sabine Begall
(2022)
The evolution and biological correlates of hand preferences in anthropoid primates
eLife 11:e77875.
https://doi.org/10.7554/eLife.77875
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4 figures, 4 tables and 4 additional files

Figures

Figure 1
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A color-coded phylogeny of hand preferences in anthropoid primates.

The strength (A) and direction (B) of laterality, expressed by the mean absolute handedness index (MeanAbsHI) and the mean handedness index (MeanHI; 0 is marked by the black bar on the color scale), respectively, calculated for each species and inferred for each tree node by maximum likelihood estimates. Silhouettes by Kai R Caspar, except Ateles (by Yan Wong, public domain) and Homo (public domain).

Figure 2
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Violin plots of hand preference distribution in 22 genera of anthropoid primates and the genus-specific expression of three potential biological correlates (ecology, habitual foraging-related tool use, and absolute brain size).

Attributions only apply to the species that represent the respective genus within our sample. Color coding: Ecology – green: arboreal, yellow: terrestrial; Habitual tool use – gray: present; white: absent. Brain size is visualized here as the log-transformed genus average of female endocranial volume.

Figure 3
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Visualization of phylogenetic generalized least squares (PGLS) coefficient estimates (including 95% confidence intervals) for the influence of brain size, tool use, and ecology on lateralization direction (A, B) as well as strength (C) in anthropoid primates.

Two models for lateralization direction were computed, one including (A), the other one excluding humans (B). The strength model encompassed humans as well (C).

Figure 4
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Various anthropoid primates engaging in the tube task.

(A) Golden lion tamarin (Leontopithecus rosalia) manipulating a small tube at Zoo Frankfurt, Germany. (B) White-handed gibbon (Hylobates lar) handling a large tube at Bioparc de Doué-la-Fontaine, France. Note that the thumb is used to probe into the tube, an insertion pattern characteristic of gibbons. (C) Yellow-breasted capuchin (Sapajus xanthosternos) engaging in the task with a medium-sized tube while adopting an erect bipedal stance at ZooParc Overloon, the Netherlands. Photographs by Kai R Caspar.

Tables

Table 1
Hand preferences of anthropoid species as recovered by the tube task.

Bold numbers indicate significant results. Results marked with an asterisk (*) remain significant after Bonferroni correction.

SpeciesN# Left (%)# Right (%)# Ambipreferent (%)MeanHIMeanAbsHISpecies direction bias (HI), p valueSpecies L/R/A distribution, p valuenGenusGenus direction bias (HI), p valueGenus L/R/A distribution, p value
Ateles fusciceps4620 (43.5)22 (47.8)4 (8.7)0.0630.7980.6180.288870.7590.031
Ateles geoffroyi2310 (43.5)11 (47.8)2 (8.7)0.0610.8290.7480.536
Ateles hybridus1813 (72.2)5 (27.8)0–0.3770.9170.0860.018
Cercocebus torquatus3113 (41.9)11 (35.5)7 (22.6)–0.0290.6650.8320.836310.8320.836
Cercopithecus diana207 (35)10 (50)3 (15)0.1780.7550.3390.836450.5720.222
Cercopithecus neglectus2514 (56)7 (28)4 (16)–0.2580.6210.0610.140
Gorilla gorilla7617 (22.4)41 (53.9)18 (23.7)0.2480.541<0.001*0.00776<0.001*0.007
Homo sapiens12712 (9.5)111 (87.4)4 (3.1)0.7610.943<0.001*<0.001*127<0.001*<0.001*
Hylobates lar3617 (47.2)16 (44.5)3 (8.3)–0.0110.6140.9240.182580.6120.125
Hylobates moloch2211 (50)8 (36.4)3 (13.6)–0.1150.7990.5400.552
Leontopithecus chrysomelas307 (23.3)12 (40)11 (36.7)0.1510.5140.1710.012730.241<0.001*
Leontopithecus chrysopygus153 (20)4 (26.7)8 (53.3)0.0390.3500.7440.001*
Leontopithecus rosalia2810 (35.7)8 (28.6)10 (35.7)0.0220.5020.8500.033
Macaca fascicularis208 (45)10 (45)2 (10)–0.0360.6840.8350.2331020.6920.863
Macaca nemestrina299 (31)11 (37.9)9 (31)0.0350.5270.7680.750
Macaca silenus3514 (40)9 (25.7)12 (34.3)–0.0510.4670.5960.328
Macaca sylvanus2412 (50)10 (41.7)2 (8.3)–0.0250.6700.8730.129
Macaca tonkeana145 (35.7)3 (21.4)6 (42.9)–0.0570.5430.7530.291
Mandrillus sphinx326 (18.8)10 (31.2)16 (50)0.0340.3890.7010.006320.7010.006
Nomascus gabriellae105 (50)2 (20)3 (30)–0.1730.6180.4650.436360.5390.805
Nomascus leucogenys269 (34.6)11 (42.3)6 (23.1)–0.0310.5550.8180.869
Pan paniscus11850 (42.4)51 (43.2)17 (14.4)0.0440.5290.4310.237654<0.001*<0.001*
Pan troglodytes536155 (28.9)266 (49.6)115 (21.5)0.1330.507<0.001*<0.001*
Papio anubis8427 (32.1)41 (48.8)16 (19.1)0.1080.5270.1020.0731080.0790.239
Papio hamadryas246 (25)7 (29.2)11 (45.8)0.0660.4080.5330.082
Pithecia pithecia75 (71.4)2 (28.6)0–0.3850.9340.3120.2217NA0.221
Pongo sp.4727 (57.5)9 (19.1)11 (23.4)–0.2250.4870.0060.012470.0060.012
Pygathrix cinerea186 (33.3)10 (55.6)2 (11.1)0.1650.4990.2680.196180.2680.196
Rhinopithecus roxellana2417 (70.8)7 (29.2)0–0.3190.7290.040<0.001*240.040<0.001*
Saimiri sciureus3621 (58.4)14 (38.9)1 (2.7)–0.1190.7570.3820.031360.3820.031
Sapajus apella2511 (44)10 (40)4 (16)–0.0280.6870.8540.961800.9220.905
Sapajus flavius2110 (47.6)7 (33.3)4 (19)–0.1300.7690.4950.755
Sapajus xanthosternos3414 (41.2)15 (44.1)5 (14.7)0.0890.6770.4920.906
Semnopithecus entellus3015 (50)7 (23.4)8 (26.6)–0.1840.5600.1100.315300.1100.315
Symphalangus syndactylus3111 (35.5)9 (29)11 (35.5)–0.0480.4820.6630.118310.6630.118
Theropithecus gelada386 (15.8)6 (15.8)26 (68.4)0.0530.2570.326<0.001*380.326<0.001*
Trachypithecus auratus85 (62.5)3 (37.5)0–0.2560.9840.4990.176260.1530.004
Trachypithecus hatinhensis1811 (61.1)7 (38.9)0–0.2480.8170.2190.023
Table 2
Conditional average of phylogenetic generalized least squares (PGLS) model coefficients for lateralization strength and direction in anthropoid primate species.

Bold numbers indicate significant results. VIF = variable inflation factor.

A: Conditional PGLS model average for lateralization direction, including humans
PredictorEstimateStd. errorVIFp value
Ecology (terrestrial lifestyle)0.1530.0721.4990.040
Tool use (present)0.1040.0821.1640.220
Log10 brain size0.0500.0431.6120.254
B: Conditional PGLS model average for lateralization direction, excluding humans
PredictorEstimateStd. errorVIFp value
Ecology (terrestrial lifestyle)
Log10 brain size
Tool use (present)		0.108
–0.020
0.003		0.056
0.037
0.068		1.419
1.405
1.098		0.067
0.601
0.962
C: Conditional PGLS model average for lateralization strength
PredictorEstimateStd. errorVIFp value
Ecology (terrestrial lifestyle)–0.1430.0671.8130.040
Tool use (present)0.0600.0701.2350.402
Log10 brain size0.0350.0471.9970.468
Table 3
Results of phylogenetic generalized least squares (PGLS) model averaging for lateralization direction (considering the inclusion and exclusion of humans) and strength.

Null models are shown in italics. Df. = degrees of freedom. AICc = second-order Akaike information criterion.

A: PGLS model for lateralization direction, including humans
ComponentsDf.AICcΔAICcWeight
Ecology3–13.6000.28
Ecology, tool use4–13.370.230.25
Brain size3–12.221.380.14
Ecology, brain size4–12.071.540.13
Ecology, tool use, brain size5–10.872.730.07
(NULL)2–10.373.230.05
Tool use, brain size4–10.203.410.05
Tool use3–9.484.120.04
B: PGLS model for lateralization direction, excluding humans
ComponentsDf.AICcΔWeight
Ecology3–30.6000.37
(NULL)2–29.371.230.20
Ecology, brain size4–28.821.780.15
Ecology, tool use4–28.012.590.10
 Tool use3–26.983.620.06
Brain size3–26.973.630.06
Ecology, tool use, brain size5–26.164.440.04
 Tool use, brain size4–24.426.180.02
C: PGLS model for lateralization strength
ComponentsDf.AICcΔAICcWeight
Ecology3–8.8400.35
Ecology, brain size4–7.850.990.21
Ecology, tool use4–7.331.510.16
(NULL)2–6.312.530.10
Ecology, brain size, tool use5–5.463.380.06
Tool use3–5.053.800.05
Brain size3–4.144.710.03
Tool use, brain size4–3.195.660.02
Table 4
Composition of the study sample, listing taxonomic identity, sex, age, and origin of subjects.

See cited studies for locations of individuals drawn from the literature.

FamilySpecies# Subjects tested# Subjects drawn from literature*Total sample# Adult females# Adult males# Subadult females# Subadult males# Unsexed subadultsLocations for subjects in this study
AtelidaeAteles fusciceps379§463011320Berlin (Zoo), Doué-la-Fontaine, Landau, Mulhouse, Munich, Osnabrück, Wuppertal
AtelidaeAteles geoffroyi91423129020Basel, Karlsruhe
AtelidaeAteles hybridus1818107010Doué-la-Fontaine, Erfurt, Frankfurt, Neuwied, Stuttgart
CallitrichidaeLeontopithecus chrysomelas30301116210Apeldoorn, Karlsruhe, Magdeburg, Mulhouse, São Paulo, Stuttgart, Wuppertal
CallitrichidaeLeontopithecus chrysopygus151569000São Paulo
CallitrichidaeLeontopithecus rosalia2828716050Apeldoorn, Basel, Doué-la-Fontaine, Duisburg, Frankfurt, Heidelberg,
Landau, Magdeburg, Münster, São Paulo
CebidaeSaimiri sciureus36**361416510
CebidaeSapajus apella25††,‡ ‡251011040
CebidaeSapajus flavius318‡ ‡2179230São Paulo
CebidaeSapajus xanthosternos1618‡ ‡341119121Apeldoorn, Magdeburg, Münster, Overloon
CercopithecidaeCercocebus torquatus1813§ §311513120Apeldoorn, Berlin (Tierpark), Karlsruhe, Münster
CercopithecidaeCercopithecus diana/roloway202097310Amsterdam, Berlin (Tierpark), Doué-la-Fontaine, Duisburg,
Heidelberg, Liberec, Mulhouse, Osnabrück
CercopithecidaeCercopithecus neglectus1213§ §,¶ ¶25812140Bekesbourne, Duisburg, Hannover, Overloon
CercopithecidaeMacaca fascicularis128***20137000Basel, Hamm, Mönchengladbach
CercopithecidaeMacaca nemestrina29291215011Arnhem, Bali, Berlin (Tierpark), Gelsenkirchen, Osnabrück
CercopithecidaeMacaca silenus35351617110Apeldoorn, Bekesbourne, Berlin (Zoo), Cologne, Dresden, Duisburg, Hodenhagen, Rheine
CercopithecidaeMacaca sylvanus159†††,‡ ‡ ‡241112010Aachen, Rheine
CercopithecidaeMacaca tonkeana†14§ § §14NANANANANA
CercopithecidaeMandrillus sphinx3232147470Amsterdam, Berlin (Zoo), Dresden, Hamm, Hodenhagen
CercopithecidaePapio anubis84¶ ¶ ¶844822590
CercopithecidaePapio hamadryas24241410000Cologne, Frankfurt, Krefeld
CercopithecidaePygathrix cinerea18****18711000
CercopithecidaeRhinopithecus roxellana24††††2485830
CercopithecidaeSemnopithecus entellus3030177420Apeldoorn, Berlin (Zoo), Gelsenkirchen, Hannover, Heidelberg
CercopithecidaeTheropithecus gelada38382011430Bekesbourne, Berlin (Tierpark), Magdeburg, Rheine, Stuttgart
CercopithecidaeTrachypithecus auratus8830320Bali, Stuttgart
CercopithecidaeTrachypithecus hatinhensis18****18810000
HominidaeGorilla gorilla76‡ ‡ ‡ ‡76221819170
HominidaeHomo sapiens127§ § § §1277156000
HominidaePan paniscus118‡ ‡ ‡ ‡118292335310
HominidaePan troglodytes536‡ ‡ ‡ ‡5361861381101020
HominidaePongo sp.47‡ ‡ ‡ ‡471712990
HylobatidaeHylobates lar1620¶ ¶ ¶ ¶,*****, †††††361418220Berlin (Tierpark), Cologne, Doué-la-Fontaine, Landau, Stuttgart,
Ulm, Wuppertal
HylobatidaeHylobates moloch222285450Bekesbourne, Lympne, Munich
HylobatidaeNomascus gabriellae64*****1053020Arnhem, Doué-la-Fontaine
HylobatidaeNomascus leucogenys /siki719¶ ¶ ¶ ¶,*****, ‡ ‡ ‡ ‡ ‡26157130Apeldoorn, Frankfurt, Osnabrück
HylobatidaeSymphalangus syndactylus1417¶ ¶ ¶ ¶, *****311211440Arnhem, Bekesbourne, Berlin (Zoo), Dortmund, Doué-la-Fontaine,
Munich, Arnhem, Hodenhagen, Osnabrück
PitheciidaePithecia pithecia7743000Basel, Dresden, Krefeld
Total ‡501128517867245832312322
  1. *

    Fulfilling our criteria.

  2. †

    Ages unknown, sex derived from given names.

  3. ‡

    Not including M. tonkeana in sex and age specific categories.

  4. §

    Nelson and Boeving, 2015.

  5. Motes Rodrigo et al., 2018.

  6. **

    Meguerditchian et al., 2012.

  7. ††

    Phillips et al., 2007.

  8. ‡ ‡

    De Andrade and Sousa, 2018.

  9. § §

    Maille et al., 2013.

  10. ¶ ¶

    Schweitzer et al., 2007.

  11. ***

    Chatagny et al., 2013.

  12. †††

    Schmitt et al., 2008.

  13. ‡ ‡ ‡

    Regaiolli et al., 2018.

  14. § § §

    Canteloup et al., 2013.

  15. ¶ ¶ ¶

    Vauclair et al., 2005.

  16. ****

    Cubí and Llorente, 2021.

  17. ††††

    Zhao et al., 2012.

  18. ‡ ‡ ‡ ‡

    Hopkins et al., 2011.

  19. § § § §

    Cochet and Vauclair, 2012.

  20. ¶ ¶ ¶ ¶

    Morino et al., 2017.

  21. *****

    Caspar et al., 2018.

  22. †††††

    Spoelstra, 2021.

  23. ‡ ‡ ‡ ‡ ‡

    Fan et al., 2017.

Additional files

Supplementary file 1

Estimates of ancestral manual lateralization patterns in anthropoid taxa.

https://cdn.elifesciences.org/articles/77875/elife-77875-supp1-v1.xlsx
Supplementary file 2

Results and visualization of Bayesian models to infer effects of sex and age cohort on individual-level hand preference patterns.

https://cdn.elifesciences.org/articles/77875/elife-77875-supp2-v1.pdf
Supplementary file 3

Species-level predictors used for phylogenetic generalized least squares (PGLS) modelling.

https://cdn.elifesciences.org/articles/77875/elife-77875-supp3-v1.xlsx
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https://cdn.elifesciences.org/articles/77875/elife-77875-transrepform1-v1.docx

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  1. Kai R Caspar
  2. Fabian Pallasdies
  3. Larissa Mader
  4. Heitor Sartorelli
  5. Sabine Begall
(2022)
The evolution and biological correlates of hand preferences in anthropoid primates
eLife 11:e77875.
https://doi.org/10.7554/eLife.77875