The phylogeny of a species-level tendency: Species heritability and possible deep origins of Bergmann's rule in tetrapods

One of the most widely recognized generalizations in biology is Bergmann's rule, the observation that, within species of birds and mammals, body size tends to be inversely related to ambient temperature. Recent studies indicate that turtles and salamanders also tend to follow Bergmann's rule, which hints that this species-level tendency originated early in tetrapod history. Furthermore, exceptions to Bergmann's rule are concentrated within squamate reptiles (lizards and snakes), suggesting that the tendency to express a Bergmann's rule cline may be heritable at the species level. We evaluated species-level heritability and early origination of Bergmann's rule by mapping size-latitude relationships for 352 species onto a tetrapod phylogeny. When the largest available dataset is used, Bergmann's rule shows significant phylogenetic signal, indicating species-level heritability. This represents one of the few demonstrations of heritability for an emergent species-level property and the first for an ecogeographic rule. When species are discretely coded as showing either Bergmann's rule or its converse, parsimony reconstructions suggest that: (1) the tendency to follow Bergmann's rule is ancestral for tetrapods, and (2) most extant species that express the rule have retained this tendency from that ancient ancestor. The first inference also generally holds when the discrete data or size-latitude correlation coefficients are analyzed using maximum likelihood, although the results are only statistically significant for some versions of the discrete analyses. The best estimates of ancestral states suggest that the traditional adaptive explanation for Bergmann's rule-conservation of metabolic heat-was not involved in the origin of the trait since that origin predates the evolution of endothermy. A more general thermoregulatory hypothesis could apply to endotherms and some ectotherms, but fails to explain why salamanders have retained Bergmann's rule. Thus, if thermoregulation underlies the origin of a Bergmann's rule tendency, this trait may have been continuously maintained while its cause changed. Alternatively, thermoregulation may not underlie Bergmann's rule in any tetrapod group. The results also suggest that many extinct groups not included in our analyses followed Bergmann's rule.