Testing the Fitness Consequences of the Thermoregulatory and Parental Care Models for the Origin of Endothermy

The origin of endothermy is a puzzling phenomenon in the evolution of vertebrates. To address this issue several explicative models have been proposed. The main models proposed for the origin of endothermy are the aerobic capacity, the thermoregulatory and the parental care models. Our main proposal is that to compare the alternative models, a critical aspect is to determine how strongly natural selection was influenced by body temperature, and basal and maximum metabolic rates during the evolution of endothermy. We evaluate these relationships in the context of three main hypotheses aimed at explaining the evolution of endothermy, namely the parental care hypothesis and two hypotheses related to the thermoregulatory model (thermogenic capacity and higher body temperature models). We used data on basal and maximum metabolic rates and body temperature from 17 rodent populations, and used intrinsic population growth rate (Rmax) as a global proxy of fitness. We found greater support for the thermogenic capacity model of the thermoregulatory model. In other words, greater thermogenic capacity is associated with increased fitness in rodent populations. To our knowledge, this is the first test of the fitness consequences of the thermoregulatory and parental care models for the origin of endothermy

Estimation of phylogenetic signal in physiological and population level variables using the K and λ parameters.

*<p>Parameters close to zero imply no phylogenetic signal. mb = body mass, BMR = basal metabolic rate, MMR = maximum metabolic rate, <i>R_max</i> = intrinsic population growth rate, T_b = body temperature.</p

Models tested in this work are presented as structural equations (for graphical representation see Figure 2).

<p>mb = body mass, MMR = maximum metabolic rate, BMR = basal metabolic rate, <i>R_max</i> = intrinsic population growth rate; T_b = body temperature.</p

Schematic of thermogenic capacity model (model VI), the best fitting model.

<p>The parameter estimated for each path and their associated probability are indicated above arrows (*** = <i>P</i><0.001 with ML, ** = <i>P</i><0.05 with ML, * = distinct from 0 based on bootstrap). The arrows’ thickness is proportional to the estimated path’s coefficient. mb = body mass, BMR = basal metabolic rate, MMR = maximum metabolic rate, <i>R_max</i> = intrinsic population growth rate; T_b = body temperature.</p

Indices used for model selection and percentage of variance explained for the response variable.

<p>χ² = Chi square value and associated probability level (where p>0.05 indicates the model could not be rejected); BIC = Bayesian Information Criterion (lower values indicate a better model), RMSEA = root means square error approximation (<0.05 is interpreted as adequate fit; Shipley, 2000), <i>r²</i> = explained variance in <i>R_max</i>.</p

Path diagrams of the evaluated causal models.

<p>The chart without shading shows all considered cause-effect relationships, colored arrows are relationships related to the tested models for endothermy while black arrows are unrelated relationships. Arrows have their corresponding number and variables. The shaded charts show the 12 models evaluated in this work, highlighting which endothermy models are represented and the involved variables. mb = body mass, BMR = basal metabolic rate, MMR = maximum metabolic rate, <i>R_max</i> = intrinsic population growth rate; T_b = body temperature. Note that for testing Koteja’s parental care model, path b5 is a correlation (indicated by bidirectional arrows), because the relationship between both variables is mediated by parental care, as proposed by the model.</p

A strong response to selection on mass-independent maximal metabolic rate without a correlated response in basal metabolic rate

Metabolic rates are correlated with many aspects of ecology, but how selection on different aspects of metabolic rates affects their mutual evolution is poorly understood. Using laboratory mice, we artificially selected for high maximal mass-independent metabolic rate (MMR) without direct selection on mass-independent basal metabolic rate (BMR). Then we tested for responses to selection in MMR and correlated responses to selection in BMR. In other lines, we antagonistically selected for mice with a combination of high mass-independent MMR and low mass-independent BMR. All selection protocols and data analyses included body mass as a covariate, so effects of selection on the metabolic rates are mass adjusted (that is, independent of effects of body mass). The selection lasted eight generations. Compared with controls, MMR was significantly higher (11.2%) in lines selected for increased MMR, and BMR was slightly, but not significantly, higher (2.5%). Compared with controls, MMR was significantly higher (5.3%) in antagonistically selected lines, and BMR was slightly, but not significantly, lower (4.2%). Analysis of breeding values revealed no positive genetic trend for elevated BMR in high-MMR lines. A weak positive genetic correlation was detected between MMR and BMR. That weak positive genetic correlation supports the aerobic capacity model for the evolution of endothermy in the sense that it fails to falsify a key model assumption. Overall, the results suggest that at least in these mice there is significant capacity for independent evolution of metabolic traits. Whether that is true in the ancestral animals that evolved endothermy remains an important but unanswered question