Age-related changes in Thyroid hormone levels of bonobos and chimpanzees indicate heterochrony in development

Behringer, Verena; Deschner, Tobias; Murtagh, Róisín; Stevens, Jeroen M. G.; Hohmann, Gottfried

doi:10.1016/j.jhevol.2013.09.008

Cited by 48 publications

(41 citation statements)

References 47 publications

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“…Thyroid hormones may directly regulate circulating IGFBP-3 levels (97, 98). Overall, the age-related decline in urinary IGFBP-3 found in this study corresponds with urinary total triiodothyronine (TT3) changes reported from bonobos and chimpanzees (68). However, the sex difference in urinary IGFBP-3 levels observed in both species was not found in urinary TT3 levels from chimpanzees.…”

Section: Discussionsupporting

confidence: 84%

“…All samples were collected non-invasively from apes housed in zoo facilities (Table S1 in Supplementary Material) in accordance with the recommendations of the NIH published standards. Details on the sampling protocol as well as the transport and storage of samples have been published previously (68). In brief, urine samples were collected directly from the urine stream or taken off the ground, only when the individual could be identified and when contamination with feces could be excluded.…”

Section: Methodsmentioning

confidence: 99%

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Sex Differences in Age-Related Decline of Urinary Insulin-Like Growth Factor-Binding Protein-3 Levels in Adult Bonobos and Chimpanzees

et al. 2016

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There is increasing interest in the characterization of normative senescence in humans. To assess to what extent aging patterns in humans are unique, comparative data from closely related species, such as non-human primates, can be very useful. Here, we use data from bonobos and chimpanzees, two closely related species that share a common ancestor with humans, to explore physiological markers that are indicative of aging processes. Many studies on aging in humans focus on the somatotropic axis, consisting of growth hormone (GH), insulin-like growth factors (IGFs), and IGF binding proteins (IGFBPs). In humans, IGFBP-3 levels decline steadily with increasing age. We used urinary IGFBP-3 levels as an alternative endocrine marker for IGF-I to identify the temporal pattern known to be related with age-related changes in cell proliferation, growth, and apoptosis. We measured urinary IGFBP-3 levels in samples from 71 bonobos and 102 chimpanzees. Focusing on samples from individuals aged 10 years or older, we found that urinary IGFBP-3 levels decline in both ape species with increasing age. However, in both species, females start with higher urinary IGFBP-3 levels than males, experience a steeper decline with increasing age, and converge with male levels around the age of 30–35 years. Our measurements of urinary IGFBP-3 levels indicate that bonobos and chimpanzees mirror human patterns of age-related decline in IGFBP-3 in older individuals (<10 years) of both sexes. Moreover, such as humans, both ape species show sex-specific differences in IGFBP-3 levels with females having higher levels than males, a result that correlates with sex differences in life expectancy. Using changes in urinary IGFBP-3 levels as a proxy for changes in GH and IGF-I levels that mark age-related changes in cell proliferation, this approach provides an opportunity to investigate trade-offs in life-history strategies in cross-sectional and in longitudinal studies, both in captivity and in the wild.

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Section: Discussionsupporting

confidence: 84%

Section: Methodsmentioning

confidence: 99%

Sex Differences in Age-Related Decline of Urinary Insulin-Like Growth Factor-Binding Protein-3 Levels in Adult Bonobos and Chimpanzees

et al. 2016

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“…Wilkins called this the “thyroid hormone hypothesis” or THH. The putatively “self‐domesticated” Pan paniscus has significantly extended periods of thyroid hormone production compared to Pan troglodytes . Wilkins (p. 438) suggested that it is possible to link the neural crest and the THH hypotheses by postulating that the “domestication syndrome” “reflects minor neural crest cell deficits as a consequence of mild decreases of thyroid hormone during embryonic development or partial loss‐of‐function mutations in the receptor(s).” A study showed that inhibition of thyroid hormone receptor action, either by knock‐down of expression or by drug inhibition, reduces neural crest cell migration …”

Section: Morphology and Human Self‐domesticationmentioning

confidence: 99%

Evaluating the self‐domestication hypothesis of human evolution

Sánchez‐Villagra

Schaik

2019

Evolutionary Anthropology

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“Self‐domestication” has been invoked to understand important aspects of human evolution, integrating physiological, behavioral, and morphological information in a novel way. It proposes that selection for reduced aggression on animals undergoing domestication provides a model for selection favoring prosocial behaviors in humans and for a set of seemingly independent features, which arose as a result of developmental correlation. We review the history of the idea and examine patterns of domestication. A lack of empirical studies on evolutionary rates and variation thwarts meaningful comparison with domestication. The neural crest hypothesis for domestication has great explanatory power but it is difficult to test. We suggest a scenario in which the morphological byproducts of domestication can act as an honest signal of reduced xenophobia. Future studies should test if alternative explanations for the features deemed to result from self‐domestication are mutually exclusive and generate data to test predictions of these hypotheses.

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“…Since in postnatal development, their concentrations tend to be higher in juvenile stages than later, the genetic changes involved in the initial stages of domestication and the development of the DS would presumably have involved, under the assumption of neoteny in domestication, longer-lasting high thyroid hormone levels in post-natal development. There is some support for such correlations: bonobos, Pan paniscus, a putatively neotenous and "self-domesticated" species of chimpanzee (Hare et al, 2012) has significantly extended periods of thyroid hormone production compared to the related nonneotenous species, Pan troglodytes (Behringer et al, 2013).…”

Section: Two Hypothesesmentioning

confidence: 99%

Revisiting two hypotheses on the “domestication syndrome” in light of genomic data

Уилкинс¹

2017

Vestn. VOGiS

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Институт теоретической биологии берлинского университета им. Гумбольдта, берлин, Германия Доместицированные млекопитающие разных видов имеют общий набор физических и физиологических признаков, которых не было у их диких предков. Совокупность этих признаков, называемая «синдро мом одомашнивания», остается загадкой со времен Чарльза Дарвина, открывшего этот феномен. В на стоящее время существуют две общие гипотезы, объясняющие это явление, которые отчасти при менимы и к другим позвоночным, например рыбам и птицам. Одну из этих гипотез мы называем гипоте зой тиреоидных гормонов (THH), а другую -гипо тезой клеток нервного гребня (NCCH). Каждая из гипотез приводит к совершенно разным выводам на уровне генетики. Основываясь на анализе по следних данных геномных исследований, имеющих отношение к обсуждаемому вопросу, мы пришли к выводу, что более обоснованной выглядит гипотеза NCCH. Тем не менее ряд наблюдений, сделанных на курах, указывает на потенциально важную роль из мененного метаболизма тиреоидных гормонов для процесса одомашнивания. Кроме того, недав ние исследования указывают на возможность существо вания дополнительных факторов одомашнивания, оказывающих влияние на приручаемость и социаль ность и не учитываемых ни одной из рассматрива емых гипотез. Кратко обсуждаются задачи, направ ленные на выявление генетических основ «синдро ма одомашнивания» и особенностей поведения, специфичных для процесса одомашнивания млеко питающих.Ключевые слова: одомашнивание животных; «син дром одомашнивания»; Чарльз Дарвин; сравни тельная геномика; неотения; клетки нервного гребня; метаболизм тиреоидных гормонов. Domesticated mammals of many different species share a set of physical and physiological traits that are not displayed by any of their wild progenitors. This suite of traits, now termed the "domestication syndrome" (DS), has been a puzzle since Charles Darwin discovered it. Two general explanations of its basis have been proposed, which in principle, could also apply to other vertebrates, such as fish and birds, whose domesticated varieties show some of its elements. The two ideas are termed here, respectively, the thyroid hormone hypothesis or the THH, and the neural crest cell hypothesis, the NCCH. The two ideas make distinctly different genetic predictions. Here, the current relevant evidence from genomics is evaluated and it is concluded that the NCCH has more support. Nevertheless, one set of observations, from chickens, suggest a potentially important role of altered thyroid metabolism in domestication. in addition, recent studies indicate the possibility of additional genetic factors in domestication, affecting tameness and sociality, that may go beyond either hypothesis. The tasks that lie ahead to fully ascertain the genetic bases of the "domes tication syndrome" and the behaviors that characterize mammalian domestication are discussed briefly.

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Age-related changes in Thyroid hormone levels of bonobos and chimpanzees indicate heterochrony in development

Cited by 48 publications

References 47 publications

Sex Differences in Age-Related Decline of Urinary Insulin-Like Growth Factor-Binding Protein-3 Levels in Adult Bonobos and Chimpanzees

Sex Differences in Age-Related Decline of Urinary Insulin-Like Growth Factor-Binding Protein-3 Levels in Adult Bonobos and Chimpanzees

Evaluating the self‐domestication hypothesis of human evolution

Revisiting two hypotheses on the “domestication syndrome” in light of genomic data

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