Within species support for the expensive tissue hypothesis: a negative association between brain size and visceral fat storage in females of the Pacific seaweed pipefish

Abstract

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the high cost of brain development and maintenance is predicted to constrain adaptive brain size evolution (the expensive tissue hypothesis, ETH). Here, we test the ETH in a teleost fish with predominant female mating competition (reversed sex roles) and male pregnancy, the pacific seaweed pipefish Syngnathus schlegeli. The relative size of the brain and other energetically expensive organs (kidney, liver, heart, gut, visceral fat, and ovary/testis) was compared among three groups: pregnant males, nonpregnant males and egg producing females. Brood size in pregnant males was unrelated to brain size or the size of any other organ, whereas positive relationships were found between ovary size, kidney size, and liver size in females. Moreover, we found that the size of energetically expensive organs (brain, heart, gut, kidney, and liver) as well as the amount of visceral fat did not differ between pregnant and nonpregnant males. However, we found marked differences in relative size of the expensive organs between sexes. Females had larger liver and kidney than males, whereas males stored more visceral fat than females. Furthermore, in females we found a negative correlation between brain size and the amount of visceral fat, whereas in males, a positive trend between brain size and both liver and heart size was found. These results suggest that, while the majority of variation in the size of various expensive organs in this species likely reflects that individuals in good condition can afford to allocate resources to several organs, the cost of the expensive brain was visible in the visceral fat content of females, possibly due to the high costs associated with female egg production.

Large-brained frogs mature later and live longer

“…), in addition to fat storage in pipefish and mammals (Tsuboi et al. ; Pontzer et al. ), and testes mass in bats (Pitnick et al.…”

“…Cognitive advantages come at a cost, specifically, large brains are metabolically expensive as brain tissue consumes more energy per unit weight than most other somatic tissues (Mink et al 1981). Consequently, negative associations between brain size and several other traits have been reported, such as gut size in primates (Navarrete et al 2011), birds (Isler and van Schaik 2009), cichlid fishes (Tsuboi et al 2015), and frogs (Liao et al 2016a), in addition to fat storage in pipefish and mammals (Tsuboi et al 2016;Pontzer et al 2016), and testes mass in bats (Pitnick et al 2006). Those negative associations are commonly interpreted as evolutionary trade-offs and used as evidence for the "costliness" of brain tissue (Aiello and Wheeler 1995).…”

“…Also, the brain metabolism of ectotherms is less responsive to ambient temperature than that of their bodies (Heath 1988). Indeed, the strongest support for a trade-off existing between brain size and other traits stems from ectotherms such as fishes (Kotrschal et al 2013;Tsuboi et al 2016) and amphibians (Liao et al 2016a). If, as hypothesized, brain tissue is relatively more costly to generate and maintain in ectotherms, this could facilitate the proposed macroevolutionary relationship between brain size and life span (see next).…”

Testing ontogenetic patterns of sexual size dimorphism against expectations of the expensive tissue hypothesis, an intraspecific example using oyster toadfish (Opsanus tau)

“…Tests for investment trade‐offs expected under the ETH have repeatedly focused on the heart, brain, and liver as candidate organs (e.g., Aiello, ; Navarrete et al., ; Warren & Iglesias, ), as these are metabolically expensive and likely subjected to evolutionary trade‐offs (Konarzewski & Diamond, ). Since the inception of the ETH, several studies have also expanded the candidate pool of potential metabolically expensive organs subjected to trade‐offs to include gonads (e.g., Bordes et al., ; Liu, Zhou, & Liao, ; Tsuboi, Shoji, Sogabe, Ahnesjö, & Kolm, ). As such our study captures tissues generally considered to be among the most likely targets for metabolic trade‐offs.…”

Relative Mass of Brain- and Intestinal Tissue in Juvenile Brown Trout: No Long-Term Effects of Compensatory Growth; with Additional Notes on Emerging Sex-Differences

“…In relation to their size, both the brain and the gut consume large amounts of energy compared to many other tissues and are thus rightly labelled as metabolically expensive tissues [9][10][11][12][13]. The specific expensive-tissue hypothesis concerning a trade-off between the brain and the gut has acquired mixed support when it has been tested in different groups of vertebrates [14][15][16][17][18][19]. More components may be involved in the trade-offs as suggested by the "energy trade-off hypothesis", a combination of the expensive-tissue hypothesis and general energy balance theory [20], incorporating other energy demanding processes such as locomotion and reproduction [21].…”