Large Brains, Small Guts: The Expensive Tissue Hypothesis Supported within Anurans

Liao, Wen Bo; Lou, Shang Ling; Zeng, Yu; Kotrschal, Alexander

doi:10.1086/688894

Cited by 68 publications

(59 citation statements)

References 57 publications

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“…Many studies have shown that there is an energetic tradeoff between brain size and other energetically expensive organs and processes [2,11,13]. However, many of these studies focused on animals with small to medium encephalization.…”

Section: Discussionmentioning

confidence: 99%

“…The direct metabolic constraints hypothesis predicts an increase in total basal metabolic rate (BMR) to pay for the energetic cost of a larger brain [5], whereas the energetic trade-off hypothesis predicts that the energetic cost of a large brain is met by reducing energy allocation to other expensive organs or functions [6,7]. Some studies in mammals have found evidence in support of the direct metabolic constraints hypothesis [5,[8][9][10], but other studies have found trade-offs between gut size and brain size in primates [6], anurans [11] and different lineages of fish [2,12], and between locomotor costs and brain mass in birds [13].…”

Section: Introductionmentioning

confidence: 99%

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The costs of a big brain: extreme encephalization results in higher energetic demand and reduced hypoxia tolerance in weakly electric African fishes

Sukhum¹,

Freiler²,

Murphy³

et al. 2016

Proc. R. Soc. B.

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A large brain can offer several cognitive advantages. However, brain tissue has an especially high metabolic rate. Thus, evolving an enlarged brain requires either a decrease in other energetic requirements, or an increase in overall energy consumption. Previous studies have found conflicting evidence for these hypotheses, leaving the metabolic costs and constraints in the evolution of increased encephalization unclear. Mormyrid electric fishes have extreme encephalization comparable to that of primates. Here, we show that brain size varies widely among mormyrid species, and that there is little evidence for a trade-off with organ size, but instead a correlation between brain size and resting oxygen consumption rate. Additionally, we show that increased brain size correlates with decreased hypoxia tolerance. Our data thus provide a non-mammalian example of extreme encephalization that is accommodated by an increase in overall energy consumption. Previous studies have found energetic trade-offs with variation in brain size in taxa that have not experienced extreme encephalization comparable with that of primates and mormyrids. Therefore, we suggest that energetic trade-offs can only explain the evolution of moderate increases in brain size, and that the energetic requirements of extreme encephalization may necessitate increased overall energy investment.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The costs of a big brain: extreme encephalization results in higher energetic demand and reduced hypoxia tolerance in weakly electric African fishes

Sukhum¹,

Freiler²,

Murphy³

et al. 2016

Proc. R. Soc. B.

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show abstract

“…After 48 h, we randomly selected 10 active females and 10 active males. Individuals were transferred to the laboratory and kept individually in a rectangular tank (0.5 m × 0.4 m × 0.4 m; Chahua, Fujian, China), and then killed by single-pithing [43,44,45,46,47]. We measured the body size (snout-vent length: SVL) of each individual to the nearest 0.01 mm with a calliper (SHANGGOMG, Shanghai, China).…”

Section: Methodsmentioning

confidence: 99%

Modulation of Gene Expression in Liver of Hibernating Asiatic Toads (Bufo gargarizans)

Jin

Yang

et al. 2018

IJMS

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Hibernation is an effective energy conservation strategy that has been widely adopted by animals to cope with unpredictable environmental conditions. The liver, in particular, plays an important role in adaptive metabolic adjustment during hibernation. Mammalian studies have revealed that many genes involved in metabolism are differentially expressed during the hibernation period. However, the differentiation in global gene expression between active and torpid states in amphibians remains largely unknown. We analyzed gene expression in the liver of active and torpid Asiatic toads (Bufo gargarizans) using RNA-sequencing. In addition, we evaluated the differential expression of genes between females and males. A total of 1399 genes were identified as differentially expressed between active and torpid females. Of these, the expressions of 395 genes were significantly elevated in torpid females and involved genes responding to stresses, as well as contractile proteins. The expression of 1004 genes were significantly down-regulated in torpid females, most which were involved in metabolic depression and shifts in the energy utilization. Of the 715 differentially expressed genes between active and torpid males, 337 were up-regulated and 378 down-regulated. A total of 695 genes were differentially expressed between active females and males, of which 655 genes were significantly down-regulated in males. Similarly, 374 differentially expressed genes were identified between torpid females and males, with the expression of 252 genes (mostly contractile proteins) being significantly down-regulated in males. Our findings suggest that expression of many genes in the liver of B. gargarizans are down-regulated during hibernation. Furthermore, there are marked sex differences in the levels of gene expression, with females showing elevated levels of gene expression as compared to males, as well as more marked down-regulation of gene-expression in torpid males than females.

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“…), and frogs (Liao et al. ), in addition to fat storage in pipefish and mammals (Tsuboi et al. ; Pontzer et al.…”

mentioning

confidence: 99%

“…; Liao et al. ) due to differences in regard to metabolic oxygen consumption of the central nervous system. Ectotherms’ brain tissue is as costly as that of homeotherms (Mink et al.…”

mentioning

confidence: 99%

Large-brained frogs mature later and live longer

Zhong

et al. 2018

Evolution

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Brain sizes vary substantially across vertebrate taxa, yet, the evolution of brain size appears tightly linked to the evolution of life histories. For example, larger brained species generally live longer than smaller brained species. A larger brain requires more time to grow and develop at a cost of exceeded gestation period and delayed weaning age. The cost of slower development may be compensated by better homeostasis control and increased cognitive abilities, both of which should increase survival probabilities and hence life span. To date, this relationship between life span and brain size seems well established in homoeothermic animals, especially in mammals. Whether this pattern occurs also in other clades of vertebrates remains enigmatic. Here, we undertake the first comparative test of the relationship between life span and brain size in an ectothermic vertebrate group, the anuran amphibians. After controlling for the effects of shared ancestry and body size, we find a positive correlation between brain size, age at sexual maturation, and life span across 40 species of frogs. Moreover, we also find that the ventral brain regions, including the olfactory bulbs, are larger in long-lived species. Our results indicate that the relationship between life history and brain evolution follows a general pattern across vertebrate clades.

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Large Brains, Small Guts: The Expensive Tissue Hypothesis Supported within Anurans

Cited by 68 publications

References 57 publications

The costs of a big brain: extreme encephalization results in higher energetic demand and reduced hypoxia tolerance in weakly electric African fishes

The costs of a big brain: extreme encephalization results in higher energetic demand and reduced hypoxia tolerance in weakly electric African fishes

Modulation of Gene Expression in Liver of Hibernating Asiatic Toads (Bufo gargarizans)

Large-brained frogs mature later and live longer

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