Brain size evolution in small mammals: test of the expensive tissue hypothesis

Brain size exhibits significant changes within and between species. Evolution of large brains can be explained by the need to improve cognitive ability for processing more information in changing environments. However, brains are among the most energetically expensive organs. Enlarged brains can impose energetic demands that limit brain size evolution. The expensive tissue hypothesis (ETH) states that a decrease in the size of another expensive tissue, such as the gut, should compensate for the cost of a large brain. We studied the interplay between energetic limitations and brain size evolution in small mammals using phylogenetically generalized least squares (PGLS) regression analysis. Brain mass was not correlated with the length of the digestive tract in 37 species of small mammals after correcting for phylogenetic relationships and body size effects. We further found that the evolution of a large brain was not accompanied by a decrease in male reproductive investments into testes mass and in female reproductive investment into offspring number. The evolution of brain size in small mammals is inconsistent with the prediction of the ETH.

Evolution of vertebrate brain size is associated with sexual traits

The expensive tissue hypothesis predicts a trade-off between investments in the brain and other energetically costly organs due to the costs associated with their growth and maintenance within the finite energy resources available. However, few studies address the strength of relationships between brain size and investments in precopulatory (ornaments and armaments) and postcopulatory (testes and ejaculates) sexual traits. Here, in a broad comparative study, we tested the prediction that the relationship between brain size and investment in sexual traits differs among taxa relative to the importance of sperm competition within them. We found that brain size was negatively correlated with sexual size dimorphism (SSD) in anurans and primates, and it tended to decrease with SSD in ungulates and cetaceans. However, brain size did not covary significantly with armaments (e.g., canine length, horn, antler, and muscle mass). Brain size was not correlated with postcopulatory sexual traits (testes and ejaculates). The intensity of covariance between brain size and precopulatory sexual traits decreased with increasing relative testis size.

Increased prenatal brain growth in a transgenic mouse model decreases cranial development: An expensive tissue hypothesis for the skull

In vertebrates, it has been argued that the development and evolution of an enlarged brain requires an increased basal metabolic rate or a compensatory reduction in the resources devoted to the formation of other metabolically costly tissues, leading to a reduction in the size of such organs. While the latter scenario is indirectly supported by comparative data, especially in primates, this inherently ontogenetic phenomenon has not been addressed in a mechanistic framework. Our experimental study investigates the relationship between brain growth and cranial development in ß-catenin transgenic mice with remarkably increased levels of prenatal neurogenesis. To evaluate associated changes in skull form and control for variation in maternal resources among mouse litters, we directly compare data from transgenic and wild-type littermates. Ossification patterns in the limbs and skull were also analyzed to control for within-subject variation in skeletal formation. Transgenic mice, with relatively larger brains, are characterized by a corresponding decrease in the degree of cranial ossification for a given age, in contrast to the presence of similar rates of postcranial ossification between transgenic and wild-type mice. This disparity is most pronounced in the neurocranial vault, which is supplied by a greater number of vessels in common with the brain than the facial skull. Mice with relatively larger brains had a decrease in cranial ossification. As modern humans are more encephalized than living apes and most extinct hominids, our findings provide unique insights into hominid evolution, particularly the “expensive tissue hypothesis” regarding energetic tradeoffs during neural and cranial development.

Increased prenatal brain growth in a transgenic mouse model decreases cranial development: An expensive tissue hypothesis for the skull

In vertebrates, it has been argued that the development and evolution of an enlarged brain requires an increased basal metabolic rate or a compensatory reduction in the resources devoted to the formation of other metabolically costly tissues, leading to a reduction in the size of such organs. While the latter scenario is indirectly supported by comparative data, especially in primates, this inherently ontogenetic phenomenon has not been addressed in a mechanistic framework. Our experimental study investigates the relationship between brain growth and cranial development in ß-catenin transgenic mice with remarkably increased levels of prenatal neurogenesis. To evaluate associated changes in skull form and control for variation in maternal resources among mouse litters, we directly compare data from transgenic and wild-type littermates. Ossification patterns in the limbs and skull were also analyzed to control for within-subject variation in skeletal formation. Transgenic mice, with relatively larger brains, are characterized by a corresponding decrease in the degree of cranial ossification for a given age, in contrast to the presence of similar rates of postcranial ossification between transgenic and wild-type mice. This disparity is most pronounced in the neurocranial vault, which is supplied by a greater number of vessels in common with the brain than the facial skull. Mice with relatively larger brains had a decrease in cranial ossification. As modern humans are more encephalized than living apes and most extinct hominids, our findings provide unique insights into hominid evolution, particularly the “expensive tissue hypothesis” regarding energetic tradeoffs during neural and cranial development.

No evidence for the expensive-tissue hypothesis in Fejervarya limnocharis

Because the brain is one of the energetically most expensive organs of animals, trade-offs have been hypothesized to exert constraints on brain size evolution. The expensive-tissue hypothesis predicts that the cost of a large brain should be compensated by decreasing size of other metabolically costly tissues, such as the gut. Here, we analyzed the relationships between relative brain size and the size of other metabolically costly tissues (i.e., gut, heart, lung, kidney, liver, spleen or limb muscles) among four Fejervarya limnocharis populations to test the predictions of the expensive-tissue hypothesis. We did not find that relative brain size was negatively correlated with relative gut length after controlling for body size, which was inconsistent with the prediction of the expensive-tissue hypothesis. We also did not find negative correlations between relative brain mass and relative size of the other energetically expensive organs. Our findings suggest that the cost of large brains in F. limnocharis cannot be compensated by decreasing size in other metabolically costly tissues.