Allen's Rule Revisited: Temperature Influences Bone Elongation During a Critical Period of Postnatal Development

Abstract

Limbs of animals raised at warm ambient temperature are significantly and permanently longer than those of siblings housed in the cold. These highly reproducible lab results closely parallel the ecogeographical tenet described by Allen's extremity size rule, which states that appendage length correlates with temperature and latitude. It is unclear what mechanisms underlie these differences and in what pattern they emerge, since the morphology is traditionally thought to reflect naturally selected genomic adaptations for thermoregulation. This study tests the a posteriori hypothesis that adult extremity length is subject to substantial modification by temperature during a brief but critical period of early postnatal development. Weanling mice (N 5 28) were divided into three groups and housed at 7 C, 21 C, or 27 C for eight weeks. Tail lengths and body mass were measured weekly. Mass did not differ at any age. Analysis of tail elongation curves revealed two distinct phases: an initial period of rapid temperature-sensitive growth in which elongation rate was directly impacted by temperature; and a second phase of continued growth in which rates were identical among groups. Comparable growth reactions occur in response to other environmental variables such as exercise, suggesting that the skeleton is most responsive to external stimuli during a window of heightened sensitivity when growth occurs most rapidly. Knowledge of the timing and degree to which growth plasticity permits mammals to immediately adjust to novel temperature conditions will be important for analyzing skeletal variation in fluctuating climates, particularly for assessing factors that may accelerate skeletal evolution at temperature extremes. Anat Rec, 296:1534Rec, 296: -1545

What makes a long tail short? Testing Allen's rule in the toque macaques of Sri Lanka

“…In support of this view, it has been shown that environmental temperature irreversibly regulates appendage length and body mass at a critical time of neonatal development (Serrat, 2013; Serrat, King, & Lovejoy, 2008; Weaver & Ingram, 1969). That is, Allan's and Bergman's rules are strongly influenced by epigenetic factors, within the bounds of a species' overall phylogenetic traits.…”

“…If these observations are correct, then epigenetic factors may also be involved in the generation of characteristic regional In support of this view, it has been shown that environmental temperature irreversibly regulates appendage length and body mass at a critical time of neonatal development (Serrat, 2013;Serrat, King, & Lovejoy, 2008;Weaver & Ingram, 1969). That is, Allan's and…”

Low temperature decreases bone mass in mice: Implications for humans

“…These data are consistent with older studies demonstrating reduced longitudinal growth, bone length, and tail length in experimental animals housed at sub‐thermoneutral temperatures (Al‐Hilli & Wright, ; Ashoub, ; Sumner, ; Weaver & Ingram, ). More recently, Serrat, King, and Lovejoy () and Serrat () found that mice housed at 7 °C had shorter bodies, tails, and limb bones than mice raised at 27 °C, despite higher food intake and no difference in body mass. Importantly, cold exposure reduced blood flow and solute transport to limb bone growth plates in vivo (Serrat et al, ; Serrat, Williams, & Farnum, ), whereas cold‐induced reductions in growth were mitigated by exercise (Serrat, Williams, & Farnum, ) and hindlimb heating (Serrat, ; Serrat et al, ).…”

Teaching an old jaw new tricks: Diet-induced plasticity in a model organism, from weaning to adulthood

“…Bernays, 1986;Meyer, 1987;Agrawal, 2001;Marchinko, 2003;Hoverman and Relyea, 2007;Muschick et al, 2011;Svanbäck and Schluter, 2012;Serrat, 2013;Standen et al, 2014). Our experiment was designed to examine how the mammalian masticatory apparatus -represented here by a model organism, the white rabbit -responds adaptively to temporal variation in food mechanical properties at different stages of the life span.…”

“…The extent to which phenotypic sensitivity to environmental cues changes during development has been examined in a variety of species and traits (Hinton and McNamara, 1984;Meyer, 1987;Bouvier, 1988;Lieberman et al, 2001;Lieberman et al, 2003;Dufty et al, 2002;Marchinko, 2003;Taborsky, 2006;Hoverman and Relyea, 2007;Kotrschal and Taborsky, 2010;Serrat, 2013). Although these studies have documented substantial variation in how plasticity varies with age, there appears to be a general tendency for plasticity to decrease as organisms mature.…”