Evidence for Expensive Tissue Hypothesis in the Asian Common Toad(Duttaphrynus melanostictus)

Li ZHAO(ORCID:0009-0000-0942-5433) ,Ying JIANG ,Duojing QIU ,Long JIN ,Chengzhi YAN ,Li ZHAO(ORCID:0009-0002-0700-4015)＊ and Wenbo LIAO＊

1 Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education),China West Normal University,Nanchong 637009,Sichuan,China

2 Key Laboratory of Artificial Propagation and Utilization in Anurans of Nanchong City,China West Normal University,Nanchong 637009,Sichuan,China

Dear Editor,

Phenotypic plasticity of an organism by modifying morphological and physiological traits responding to diverse environments is widely recognized across animal taxa(Muñoz-Muñozet al.,2021;Donihueet al.,2021;Giacominiet al.,2022;Zamora-Camachoet al.,2022;Jianget al.,2022;Chenet al.,2023).The brain,as a critical phenotypic trait,displays a significant variation in size among different species(Striedter,2006).Prior research has demonstrated that brain size can serve as an indicator of cognitive abilities and the capacity for local adaptation in response to changing environments (Liaoet al.,2022;Jianget al.,2023).For instance,relatively larger brains are associated with enhanced cognitive abilities and greater behavioral flexibility(Chenet al.,2023),facilitating the effective localization of diverse and dispersed food sources in fluctuating environments.Nonetheless,the brain is also one of the most energyconsuming organs in vertebrates and may not be temporarily reducible in size(Minket al.,1981),thereby constraining the evolution of brain size under periodic food scarcity(Liaoet al.,2016).Two primary hypotheses have been proposed to elucidate the relationships between brain size and the size of other organs.The expensive tissue hypothesis (ETH)postulates that as the energetic investments of brain in an organism increase,there will be a corresponding decrease in the allocation of energy to the digestive tract,thereby leading to an inverse relationship between brain size and the length of the digestive tract (Aiello and Wheeler,1995).Subsequently,the ETH has been expanded to encompass other expensive tissues (e.g.,heart,livers and limb muscles).The energetic trade-off hypothesis (ETOH) states that the brain and other high energy-consuming tissues should exhibit negative correlations because the energy consumed for brain development should be compensated by a reduction in the energy allocated to body maintenance,exercise or reproduction (Isler and van Schaik,2006).Indeed,there is supporting evidence for the evolutionary trade-off between two organs across various animal groups(Isler and van Schaik,2006;Liaoet al.,2016).

We first examined the ETH in the Asian common toad(Duttaphrynus melanostictus) Through an analysis of the association between brain size and digestive tract length.The general linear regression models unveiled a statistically significant negative correlation between relative brain size and relative digestive tract length(β=-0.221,t=-3.911,P=0.001;Table S1,Figure 1A) when accounting for the influences of body mass and sex.The results of the multivariate linear regression models additionally uncovered a significant negative correlation between relative brain size and relative length of digestive tract (β=-0.232;t=-2.812;P=0.006;Table S2).Supporting brain is an organ that demands a high amount of energy (Minket al.,1981),and periodic food scarcity will limit the enlargement of brain size.In addition,the digestive tract plays a vital role in energy acquisition,and thus a lengthier digestive tract may enhance the efficiency of resource uptake(Sibly,1981).Indeed,there is evidence that less efficient resource uptake limits increased brain size in anurans(Liaoet al.,2023).Hence,the constrain of the food resources will promote longer digestive tract and smaller brain size,which result in a trade-off between digestive tract and brain size inD.melanostictus,following the prediction of the ETH.

Figure 1 Relationship between relative brain size and relative length of digestive tract(A),relative heart size(B)and relative kidney size(C)in the Asian common toad (Duttaphrynus melanostictus).

We then tested the ETOH in this species by analyzing the associations between brain size and the sizes of other organs,such as the heart,lung,gallbladder,liver,spleen,kidney,forelimb muscle,and hindlimb muscle.We found negative correlations between relative brain size and relative heart size(β=-0.138,t=-3.945,P＜0.001;Figure 1B) and relative kidney size(β=-0.114,t=-2.448,P=0.016;Table S2;Figure 1C).The ETOH has been substantiated in both homeothermic vertebrates(Navarreteet al.,2011)and ectothermic vertebrates(Liaoet al.,2016).The negative correlation between heart size and brain size suggested that larger heart was likely to provide energy for body by declining investment in brain under unstable environments.The kidney consumes energy and oxygen to properly perform the operations of filtering the blood and balancing metabolism in the body (Yang,2002).Therefore,a trade-off between brain size and kidney size inD.melanostictussuggested that unstable environments possibly promoted more energy investment in kidney for metabolic wastes and biological pH balance by decreasing energy investment in brain.No negative correlations were detected between brain size and the sizes of the lungs,gallbladders,livers,spleens,forelimb muscles and hindlimb muscles,suggesting that these organs do not exhibit an energetic trade-off with the brain.

Finally,we tested the energetic trade-offs between the other organs.We found negative correlations between relative heart size and relative liver size and between relative forelimb muscles and relative digestive tract length(Table S3).Since all organs of an organism interact with each other,the energy cost of one energy-demanding tissue did not necessarily affect another energy-demanding tissue.Instead,it may affect the investments in several other energetically expensive tissues(Isler and van Schaik,2006).Meanwhile,the ETOH predicts negative correlations between relative size of the other energetically expensive organs (e.g.,heart,livers,lungs and limb muscles;Liaoet al.,2016).Here,the observed negative correlations between heart size and liver size and between forelimb muscles and digestive tract length inD.melanostictus,align with the prediction of the ETOH.

Our study offers partial support for the prediction of the ETH and ETOH.We observed a negative correlation between relative brain size and relative length of digestive tract.Moreover,our findings revealed negative correlations between relative brain size and relative sizes of heart and kidneys,supporting the view that energy consumed for brain development is compensated by a reduction in the size of other metabolically expensive organs.Our study contributes to the theoretical understandings of the ETH and ETOH in anurans and provides for further investigations into the evolutionary relationships between brain size and energic expensive organs size.

AcknowledgementsThis research has received funding from the National Natural Science Foundation of China(32300358,32370456)and the Key Project of Natural Science Foundation of Sichuan Province (22NSFSC0011).