Factors influencing infant sex ratio in howler monkeys (Alouatta spp.): A literature review and analysis.
competition
infant sex ratio
population growth
rainfall
sex allocation
sex ratio
Journal
American journal of physical anthropology
ISSN: 1096-8644
Titre abrégé: Am J Phys Anthropol
Pays: United States
ID NLM: 0400654
Informations de publication
Date de publication:
05 2020
05 2020
Historique:
received:
27
09
2019
revised:
11
02
2020
accepted:
19
02
2020
pubmed:
7
3
2020
medline:
9
1
2021
entrez:
7
3
2020
Statut:
ppublish
Résumé
Frequency-dependent selection is expected to maintain infant sex ratios around parity over evolutionary time. However, over ecological time periods, infant sex ratios vary, and it has been proposed that this variation may reflect adaptive processes. In primates, there are consistent patterns of variation in infant sex ratios, although their adaptive significance remains contentious. In addition to design issues, contrasting results could have derived across primates from variation in the fitness benefits accrued through sons or daughters associated with the specific social, ecological, and demographic context of populations. Thus, different sex allocation tactics could occur within species over time and space. We reviewed the literature to describe variation in infant sex ratio in howler monkeys (genus Alouatta) and to examine whether such a variation could be associated with adaptive sex allocation. We found 26 studies that provided data for this review. These studies yielded 96 infant sex reports, corresponding to 1,477 sexed infants. Infant sex ratio across howler monkey species tends to parity, but females produce more sons under high group densities and more daughters when rainfall increases. Based on these results, as well as on information on howler monkey dispersal patterns, demography, and within-group genetic relatedness, we speculate that, depending on population growth stage, sex allocation is explained by (a) local resource enhancement, that is, more cooperative philopatric daughters are produced when populations are growing; and (b) local resource competition, that is, more dispersing sons are produced when populations are saturated. Thus, there is evidence suggestive of adaptive variation in infant sex ratios in howler monkeys.
Types de publication
Journal Article
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
48-57Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Aars, J., Andreassen, H. P., & Ims, R. A. (1995). Root voles: Litter sex ratio variation in fragmented habitat. Journal of Animal Ecology, 64, 459-472.
Abbott, D. H., Keverne, E. B., Bercovitch, F. B., Shively, C. A., Mendoza, S. P., Saltzman, W., … Sapolsky, R. M. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior, 43, 67-82.
Altmann, M., & Altmann, J. (1991). Models of status-correlated bias in offspring sex ratio. American Naturalist, 137, 556-566.
Bartoń, K. (2019). ‘MuMIn’: Multi-model inference. R package version 1.43.6. https://cran.r-project.org/web/packages/MuMIn/index.html
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2019). ‘lme4’ linear mixed-effects models using ‘Eigen’ and S4. R package version 1.1-21. https://cran.r-project.org/web/packages/lme4/index.html
Berkeley, E. V., & Linklater, W. L. (2010). Annual and seasonal rainfall may influence progeny sex ratio in the black rhinoceros. South African Journal of Wildlife Research, 40, 53-57.
Bezanson, M., & McNamara, A. (2019). The what and where of primate field research may be failing primate conservation. Evolutionary Anthropology, 4, 166-178.
Bodmer, W., & Edwards, A. W. F. (1960). Natural selection and the sex ratio. Annals of Human Genetics, 24, 239-244.
Boinski, S., Ehmke, E., Kauffman, L., Schet, S., & Vreedzaam, A. (2005). Dispersal patterns among three species of squirrel monkeys (Saimiri oerstedii, S. boliviensis and S. sciureus): II. Within-species and local variation. Behaviour, 142, 633-677.
Bonier, F., Martin, P. R., & Wingfield, J. C. (2007). Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird. Behavioral Ecology, 18, 1045-1050.
Booksmythe, I., Mautz, B., Davis, J., Nakagawa, S., & Jennions, M. D. (2017). Facultative adjustment of the offspring sex ratio and male attractiveness: A systematic review and meta-analysis. Biological Reviews, 92, 108-134.
Borowik, T., & Jędrzejewska, D. (2017). Heavier females produce more sons in a low-density population of red deer. Journal of Zoology, 302, 57-62.
Brown, G. R. (2001). Sex-biased investment in nonhuman primates: Can Trivers and Willard's theory be tested? Animal Behaviour, 61, 683-694.
Burley, N. (1981). Sex ratio manipulation and selection for attractiveness. Science, 211, 721-722.
Burley, N. (1986). Sex-ratio manipulation in color-banded populations of zebra finches. Evolution, 40, 1191-1206.
Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference. New York: Springer.
Calegaro-Marques, C., & Bicca-Marques, J. C. (1996). Emigration in a black howling monkey group. International Journal of Primatology, 17, 229-237.
Cameron, E. Z., Lemons, P. R., Bateman, P. W., & Bennett, N. C. (2008). Experimental alteration of litter sex ratios in a mammal. Proceedings of the Royal Society B, 275, 323-327.
Cañadas-Santiago, S., Dias, P. A. D., Garau, S., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Rangel-Negrín, A. (2019). Behavioral and physiological stress responses to local spatial disturbance and human activities by howler monkeys at Los Tuxtlas, Mexico. Animal Conservation. https://doi.org/10.1111/acv.12541
Cano-Huertes, B., Rangel-Negrín, A., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Dias, P. A. D. (2017). Reproductive energetics of female mantled howler monkeys (Alouatta palliata). International Journal of Primatology, 5, 942-961.
Chason, R. J., McLain, A. C., Sundaram, R., Chen, Z., Segars, J. H., Pyper, C., & Louis, G. M. B. (2012). Preconception stress and the secondary sex ratio: A prospective cohort study. Fertility and Sterility, 98, 937-941.
Clark, A. B. (1978). Sex-ratio and local resource competition in a prosimian primate. Science, 201, 163-165.
Clarke, M. R., Zucker, E. L., Ford, R. T., & Harrison, R. M. (2007). Behavior and endocrine concentrations do not distinguish sex in monomorphic juvenile howlers (Alouatta palliata). American Journal of Primatology, 69, 477-484.
Clutton-Brock, T. (1991). The evolution of parental care. Princeton: Princeton University Press.
Cockburn, A., Legge, S., & Double, M. C. (2002). Sex ratios in birds and mammals: Can the hypotheses be disentangled? In I. C. Hardy (Ed.), Sex ratios: Concepts and research methods (pp. 266-286). Cambridge: Cambridge University Press.
Cortés-Ortiz, L., Rylands, A. B., & Mittermeier, R. A. (2015). The taxonomy of howler monkeys: Integrating old and new knowledge from morphological and genetic studies. In M. Kowalewski, P. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Adaptive radiation, systematics, and morphology (pp. 55-84). New York: Springer.
Crawley, M. J. (2013). The R book (2nd ed.). West Sussex: Wiley.
Cristóbal Azkarate, J., Dunn, J. C., Domingo-Balcells, C., & Veà, J. J. (2017). A demographic history of a population of howler monkeys (Alouatta palliata) living in a fragmented landscape in Mexico. PeerJ, 5, e3547.
Crockett, C. M. (1984). Emigration by female red howler monkeys and the case for female competition. In M. F. Small (Ed.), Female primates: Studies by women primatologists (pp. 159-173). New York: Liss.
Crockett, C. M. (1996). The relation between red howler monkey (Alouatta seniculus) troop size and population growth in two habitats. In M. A. Norconk, A. L. Rosenberger, & P. A. Garber (Eds.), Adaptive radiations of neotropical primates (pp. 489-510). New York: Plenum.
Crockett, C. M. (1998). Conservation biology of the genus Alouatta. International Journal of Primatology, 19, 549-578.
Crockett, C. M., & Janson, C. H. (2000). Infanticide in red howlers: Female group size, male membership and a possible link to folivory. In C. P. van Schaik & C. H. Janson (Eds.), Infanticide by males and its implications (pp. 75-98). Cambridge University Press: Cambridge.
Crockett, C. M., & Pope, T. R. (1993). Consequences of sex differences in dispersal for juvenile red howler monkeys. In M. E. Pereira & L. A. Fairbanks (Eds.), Juvenile primates: Life history, development and behavior (pp. 104-118). New York: Oxford University Press.
Crockett, C. M., & Rudran, R. (1987). Red howler monkey birth data II: Interannual, habitat, and sex comparisons. American Journal of Primatology, 13, 369-384.
Darwin, C. R. (1871). The descent of man, and selection in relation to sex. London: John Murray.
Di Fiore, A., Link, A., & Campbell, C. J. (2010). The atelines: Behavioral and socioecological diversity in a New World radiation. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. K. Bearder, & R. Stumpf (Eds.), Primates in perspective (2nd ed., pp. 155-188). Oxford: Oxford University Press.
Di Fiore, A., Link, A., Schmitt, C. A., & Spehar, S. (2009). Dispersal patterns in sympatric woolly and spider monkeys: Integrating molecular and observational data. Behaviour, 146, 437-470.
Dias, P. A. D., Coyohua-Fuentes, A., Canales-Espinosa, D., & Rangel-Negrín, A. (2015). Group structure and dynamics in black howlers (Alouatta pigra): A 7-year perspective. International Journal of Primatology, 36, 311-331.
Dias, P. A. D., & Rangel-Negrín, A. (2015). Diets of howler monkeys. In M. M. Kowalewski, P. A. Garber, L. O. Cortés, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology, and conservation (pp. 21-56). New York: Springer.
Dias, P. A. D., Coyohua-Fuentes, A., Canales-Espinosa, D., & Rangel-Negrín, A. (2018a). Maternal condition determines infant sex in black howler monkeys (Alouatta pigra) in Mexico. In B. Urbani, M. M. Kowalewski, R. G. Teixeira da Cunha, S. Torre, & L. Cortés-Ortiz (Eds.), La primatología en Latinoamérica 2 (pp. 519-529). Caracas: Instituto Venezolano de Investigaciones Científicas.
Dias, P. A. D., Cano-Huertes, B., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Rangel-Negrín, A. (2018b). Maternal condition and maternal investment during lactation in mantled howler monkeys. American Journal of Physical Anthropology, 167, 178-184.
Douhard, M. (2018). The role of fathers in mammalian sex allocation. Mammal Review, 48, 67-74.
Edwards, A. M., & Cameron, E. Z. (2014). Forgotten fathers: Paternal influences on mammalian sex allocation. Trends in Ecology and Evolution, 29, 158-164.
Emlen, S. T., Emlen, J. M., & Levin, S. A. (1986). Sex-ratio selection in species with helpers-at-the-nest. American Naturalist, 127, 1-8.
Fisher, R. (1958). The genetical theory of natural selection (2nd ed.). London: The Clarendon Press.
Fox, J., Weisberg, S., & Price, B. (2019). ‘car’: Companion to applied regression. R package version 3.0-3. https://cran.r-project.org/web/packages/car/index.html
Frank, S. A. (1990). Sex allocation theory for birds and mammals. Annual Review of Ecology and Systematics, 21, 13-55.
Gómez-Espinosa, R., Rangel-Negrín, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Dias, P. A. D. (2014). Glucocorticoid response in mantled howlers (Alouatta palliata) in relation to energetic and psychosocial stressors. American Journal of Primatology, 76, 362-373.
Gutiérrez-Adán, A., Granados, J., Pintado, B., & De la Fuente, J. (2001). Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reproduction, Fertility and Development, 13, 361-365.
Hamilton, W. D. (1979). Wingless and fighting males in fig wasps and other insects. In M. S. Blum & N. A. Blum (Eds.), Reproductive competition and sexual selection in insects (pp. 167-220). New York: Academic Press.
Hewison, A. J. M., & Gaillard, J. M. (1999). Successful sons or advantaged daughters? The Trivers-Willard model and sex biased maternal investment in ungulates. Trends in Ecology and Evolution, 14, 229-234.
Hogg, J. C., Hass, C. C., & Jenni, D. A. (1992). Sex-biased maternal expenditure in Rocky Mountain bighorn sheep. Behavioral Ecology and Sociobiology, 31, 243-251.
Horwich, R. H., Brockett, R. C., James, R. A., & Jones, C. A. (2001). Population structure and group productivity of the Belizean black howling monkey (Alouatta pigra): Implications for female socioecology. Primate Report, 61, 47-65.
Johnson, C. N. (1988). Dispersal and the sex ratio at birth in primates. Nature, 332, 726-728.
Julliard, R. (2000). Sex-specific dispersal in spatially varying environments leads to habitat-dependent evolutionarily stable offspring sex ratios. Behavioral Ecology, 11, 421-428.
Kokko, H., & Jennions, M. (2008). Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology, 21, 919-948.
Kokko, H., & Rankin, D. J. (2006). Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philosophical Transactions of the Royal Society of London B, 361, 319-334.
Kolman, W. (1960). The mechanism of natural selection on the sex ratio. American Naturalist, 94, 373-377.
Kowalewski, M. M., Garber, P. A., Cortés-Ortiz, L., Urbani, B., & Youlatos, D. (2015a). Howler monkeys: Adaptive radiation, systematics, and morphology. New York: Springer.
Kowalewski, M. M., Garber, P. A., Cortés-Ortiz, L., Urbani, B., & Youlatos, D. (2015b). Howler monkeys: Behavior, ecology and conservation. New York: Springer.
Kruuk, L. E. B., Clutton-Brock, T. H., Albon, S. D., Pemberton, J. M., & Guinness, F. E. (1999). Population density affects sex ratio variation in red deer. Nature, 399, 459-461.
Lavoie, M. D., Tedeschi, J. N., García-González, F., & Firman, R. C. (2019). Exposure to male-dominated environments during development influences sperm sex ratios at sexual maturity. Evolution Letters, 3-4, 392-402.
Law, P. R., Fike, B., & Lent, P. C. (2014). Birth sex in an expanding black rhinoceros (Diceros bicornis minor) population. Journal of Mammalogy, 95, 349-356.
Lecompte, E., Bouanani, M. A., de Thoisy, B., & Crouau-Roy, B. (2017). How do rivers, geographic distance, and dispersal behavior influence genetic structure in two sympatric New World monkeys? American Journal of Primatology, 79, 22660.
Lessells, C. M., & Avery, M. I. (1987). Sex-ratio selection in species with helpers at the nest: Some extensions of the repayment model. American Naturalist, 129, 610-620.
Lewis, S. L., Sonke, B., Sunderland, T., Begne, S. K., López-González, G., van der Heijden, G. M. F., … Zemagho, L. (2013). Aboveground biomass and structure of 260 African tropical forests. Philosophical Transactions of the Royal Society of London B, 368, 20120295.
Malhi, Y., Baker, T. R., Phillips, O. L., Almeida, S., Alvarez, E., Arroyo, L., … Lloyd, J. (2004). The above-ground coarse wood productivity of 104 Neotropical forest plots. Global Change Biology, 10, 563-591.
Martin, J. G. A., & Festa-Bianchet, M. (2011). Sex ratio bias and reproductive strategies: What sex to produce when? Ecology, 92, 441-449.
Martínez-Mota, R., Valdespino, C., Sánchez-Ramos, M. A., & Serio-Silva, J. C. (2007). Effects of forest fragmentation on the physiological stress response of black howler monkeys. Animal Conservation, 10, 374-379.
Minhós, T., Nixon, E., Sousa, C., Vicente, L. M., Da Silva, M. F., Sá, R., & Bruford, M. W. (2013). Genetic evidence for spatio-temporal changes in the dispersal patterns of two sympatric African colobine monkeys. American Journal of Physical Anthropology, 150, 464-474.
Moore, E. P. B., Hayward, M., & Robert, K. A. (2015). High density, maternal condition, and stress are associated with male-biased sex allocation in a marsupial. Journal of Mammalogy, 96, 1203-1213.
Moura, A. C. D. A., & McConkey, K. R. (2007). The capuchin, the howler, and the caatinga: Seed dispersal by monkeys in a threatened Brazilian forest. American Journal of Primatology, 69, 220-226.
Nidiffer, M. D., & Cortés-Ortiz, L. (2015). Intragroup genetic relatedness in two howler monkey species (Alouatta pigra and A. palliata): Implications for understanding social systems and dispersal. American Journal of Primatology, 77, 1333-1345.
Oklander, L. I., Kowalewski, M. M., & Corach, D. (2010). Genetic consequences of habitat fragmentation in black-and-gold howler (Alouatta caraya) populations from northern Argentina. International Journal of Primatology, 31, 813-832.
Opie, C., Atkinson, Q. D., Dunbar, R. I. M., & Shultz, S. (2013a). Male infanticide leads to social monogamy in primates. Proceedings of the National Academy of Sciences USA, 110, 13328-13332.
Packer, C., Collins, D. A., & Eberly, L. E. (2000). Problems with primate sex ratios. Proceedings of the Royal Society of London B, 355, 1627-1635.
Pen, I., & Weissing, F. J. (2000). Sex-ratio optimization with helpers at the nest. Proceedings of the Royal Society of London B, 267, 539-543.
Perret, M. (1990). Influence of social factors on sex ratio at birth, maternal investment and young survival in a prosimian primate. Behavioral Ecology and Sociobiology, 27, 447-454.
Perret, M. (1996). Manipulation of sex ratio at birth by urinary cues in a prosimian primate. Behavioral Ecology and Sociobiology, 38, 259-266.
Pope, T. R. (1990). The reproductive consequences of male cooperation in the red howler monkey. Behavioral Ecology and Sociobiology, 27, 439-446.
Pope, T. R. (2000). Reproductive success increases with degree of kinship in cooperative coalitions of female red howler monkeys (Alouatta seniculus). Behavioral Ecology and Sociobiology, 48, 253-267.
Quesada, C. A., Lloyd, J., Schwarz, M., Baker, T. R., Phillips, O. L., Patino, S., … Ramírez, H. (2009). Regional and large-scale patterns in Amazon forest structure and function are mediated by variations in soil physical and chemical properties. Biogeosciences Discussions, 6, 3993-4057.
R Core Team. (2019). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/
Raguet-Schofield, M., & Pavé, R. (2015). An ontogenetic framework for Alouatta: Infant development and evaluating models of life history. In M. M. Kowalewski, P. A. Garber, L. Cortés, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Adaptive radiation, systematics, and morphology (pp. 289-316). New York: Springer.
Rangel-Negrín, A., Coyohua-Fuentes, A., Canales-Espinosa, D., Chavira-Ramírez, D. R., & Dias, P. A. D. (2018). Maternal glucocorticoid levels as a sex allocation mechanism in black howler monkeys. Journal of Zoology, 304, 124-131.
Rangel-Negrín, A., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Dias, P. A. D. (2014). Primates living outside protected habitats are more stressed: The case of black howler monkeys in the Yucatán peninsula. PLoS One, 9, e112329.
Rangel-Negrín, A., Coyohua-Fuentes, A., Chavira-Ramírez, D. R., Canales-Espinosa, D., & Dias, P. A. D. (2018). Energetic constraints on the reproduction of female mantled howlers. American Journal of Primatology, 80, e22925, 1-9.
Reinhold, K. (1996). Sex-ratio selection with asymmetrical migration of the sexes can lead to an uneven sex ratio. Oikos, 75, 15-19.
Rimbach, R., Link, A., Heistermann, M., Gómez-Posada, C., Galvis, N., & Heymann, E. W. (2013). Effects of logging, hunting, and forest fragment size on physiological stress levels of two sympatric ateline primates in Colombia. Conservation Physiology, 1, cot031.
Robinson, J. G., & O'Brien, T. G. (1991). Adjustment in birth sex ratio in wedge-capped capuchin monkeys. American Naturalist, 138, 1173-1186.
Rudran, R., & Fernández-Duque, E. (2003). Demographic changes over thirty years in a red howler population in Venezuela. International Journal of Primatology, 24, 925-947.
Rumiz, D. I. (1992). Effects of demography, kinship, and ecology on the behavior of the red howler monkey, Alouatta seniculus. (Unpublished PhD dissertation) University of Florida, Gainesville.
Rutberg, A. T. (1986). Lactation and the foetal sex ratios in American bison. American Naturalist, 127, 89-94.
Ryan, C. P., Anderson, W. G., Berkvens, C., & Hare, J. F. (2014). Maternal gestational cortisol and testosterone are associated with trade-offs in offspring sex and number in a free-living rodent (Urocitellus richardsonii). PLoS One, 9, e111052.
Ryan, C. P., Anderson, W. G., Gardiner, L. E., & Hare, J. F. (2012). Stress-induced sex ratios in ground squirrels: Support for a mechanistic hypothesis. Behavioral Ecology, 23, 160-167.
Saltz, D. (2001). Progeny sex ratio variation in ungulates: Maternal age meets environmental perturbation of demography. Oikos, 94, 377-384.
Schindler, S., Gaillard, J. M., Grüning, A., Neuhaus, P., Traill, L. W., Tuljapurkar, S., & Coulson, T. (2005). Sex-specific demography and generalization of the Trivers-Willard theory. Nature, 526, 249-252.
Schino, G. (2004). Birth sex ratio and social rank: Consistency and variability within and between primate groups. Behavioral Ecology, 15, 850-856.
Schwanz, L. E., & Robert, K. A. (2014). Proximate and ultimate explanations of mammalian sex allocation in a marsupial model. Behavioral Ecology and Sociobiology, 68, 1085-1096.
Schwarz, M. P. (1988). Local resource enhancement and sex ratios in a primitively social bee. Nature, 331, 346-348.
Sheldon, B. C., & West, S. A. (2004). Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals. American Naturalist, 163, 40-54.
Silk, J. B. (1984). Local resource competition and the evolution of male-biased sex ratios. Journal of Theoretical Biology, 108, 203-213.
Silk, J. B., & Brown, G. R. (2004). Sex ratios in primate groups. In P. M. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 253-265). Cambridge: Cambridge University Press.
Silk, J. B., & Brown, G. R. (2008). Local resource competition and local resource enhancement shape primate birth sex ratios. Proceedings of the Royal Society of London B, 275, 1761-1765.
Silk, J. B., Willoughby, E., & Brown, G. R. (2005). Maternal rank and local resource competition do not predict birth sex ratios in wild baboons. Proceedings of the Royal Society of London B, 272, 569-574.
Sterck, E. H. M., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioral Ecology and Sociobiology, 41, 291-309.
Strier, K. B., Mendes, S. L., & Santos, R. R. (2001). Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus). American Journal of Primatology, 55, 87-100.
Tanaka, Y., Fukano, Y., & Nakamura, M. (2019). Effect of paternal age on the birth sex ratio in captive populations of aye-aye (Daubentonia madagascariensis [Gmelin]). Zoo Biology, 38, 389-392.
Taylor, P. D. (1994). Sex ratio in a stepping-stone population with sex-specific dispersal. Theoretical Population Biology, 45, 203-218.
Ter Steege, H., Pitman, N., Sabatier, D., Castellanos, H., Van der Hout, P., Daly, D. C., … Morawetz, W. (2003). A spatial model of tree α-diversity and β-density for the Amazon region. Biodiversity and Conservation, 12, 2255-2277.
Thorington, R. W., Jr., Ruiz, J. C., & Eisenberg, J. F. (1984). A study of a black howling monkey (Alouatta caraya) population in northern Argentina. American Journal of Primatology, 6, 357-366.
Toledo, M., Poorter, L., Peña-Claros, M., Alarcón, A., Balcázar, J., Leaño, C., … Bongers, F. (2011). Climate is a stronger driver of tree and forest growth rates than soil and disturbance. Journal of Ecology, 99, 254-264.
Trivers, R. L., & Willard, D. E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science, 179, 90-92.
Van Belle, S., Estrada, A., & Di Fiore, A. (2014). Kin-biased spatial associations and social interactions in male and female black howler monkeys (Alouatta pigra). Behaviour, 151, 2029-2057.
Van Belle, S., Estrada, A., Strier, K. B., & Di Fiore, A. (2012). Genetic structure and kinship patterns in a populations of black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico. American Journal of Primatology, 74, 948-957.
van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & F. A. Foley (Eds.), Comparative socioecology. The behavioural ecology of humans and other mammals (pp. 195-218). Oxford: Blackwell.
van Schaik, C. P., & Hrdy, S. B. (1991). Intensity of local resource competition shapes the relationship between maternal rank and sex ratios at birth in cercopithecine primates. American Naturalist, 138, 1555-1562.
Weladji, R. B., & Laflamme-Mayer, K. (2010). Influence of environmental conditions on sex allocation in the black rhinoceros population of Mkhuze Game Reserve, South Africa. African Journal of Ecology, 49, 471-480.
Wells, C. P., & Van Vuren, D. H. (2017). Female kin density affects offspring sex ratio in an asocial mammal, the golden-mantled ground squirrel, Callospermophilus lateralis. Animal Behaviour, 134, 71-77.
Wilson, D. S., & Colwell, R. K. (1981). Evolution of sex ratio in structured demes. Evolution, 35, 882-897.