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The adaptive potential of livestock under a warming climate is increasingly relevant in relation to the growing pressure of global food security. Studies on heat tolerance demonstrate the interplay of adaptation and acclimatization in functional traits, for example, a reduction in body size and enhanced tolerance in response to a warming climate. However, current lack of understanding of functional traits and phylogenetic history among phenotypically distinct populations constrains predictions of climate change impact. Here, we demonstrate evidence of parallel evolution in adaptive tolerance to heat stress in dwarf cattle breeds (DCB, Bos taurus indicus) and compare their thermoregulatory responses with those in standard size cattle breeds (SCB, crossbred, Bos taurus indicus × Bos taurus taurus). We measured vital physiological, hematological, biochemical, and gene expression changes in DCB and SCB and compared the molecular phylogeny using mitochondrial genome (mitogenome) analysis. Our results show that SCB can acclimatize in the short term to higher temperatures but reach their tolerance limit under prevailing tropical conditions, while DCB is adapted to the warmer climate. Increased hemoglobin concentration, reduced cellular size, and smaller body size enhance thermal tolerance. Mitogenome analysis revealed that different lineages of DCB have evolved reduced size independently, as a parallel adaptation to heat stress. The results illustrate mechanistic ways of dwarfing, body size‐dependent tolerance, and differential fitness in a large mammal species under harsh field conditions, providing a background for comparing similar populations during global climate change. These demonstrate the value of studies combining functional, physiological, and evolutionary approaches to delineate adaptive potential and plasticity in domestic species. We thus highlight the value of locally adapted breeds as a reservoir of genetic variation contributing to the global domestic genetic resource pool that will become increasingly important for livestock production systems under a warming climate. As body size affects thermoregulation and energetics, declining body size has been documented as a universal response to climate warming. Here, we demonstrate parallel evolution of reduced body size and thermal tolerance in the world's smallest breed of cattle—Vechur. Using comparative size‐dependent thermoregulatory, metabolic, and phylogenetic responses, we illustrate the ecological and evolutionary consequences of body size shifts in domestic cattle. [ABSTRACT FROM AUTHOR]

Simple Summary: An understanding of the way that animals respond to heat stress is key to the development of adaptation and mitigation strategies for a changing climate. The response of mammals to heat exposure involves changes at every level of organization from molecular and cellular to systemic and behavioral. The concert of events involves many genes and gene products. The Na+/K+ ATPase ∝1 (ATP1A1), a product of the ATP1A1 gene, is important for the response to heat because it determines the activity of the Na+/K+ pump that is ubiquitous in cell membranes. It was shown recently that ATP1A1 is important in combating the oxidative stress that a cell faces and that it modulates the Src signaling pathway that is involved in the response to many stressors. Vechur cattle (dwarf Bos taurus indicus) are well known for their adaptability to the tropical heat and humidity that persists in their native state of Kerala, India. We here analyze the comparative expression profile of the ATP1A1 gene in heat-tolerant Vechur and Kasaragod (another dwarf B. t. indicus) cattle and a heat-intolerant crossbreed (B. t. taurus × B. t. indicus) and characterize the sequence of ATP1A1 mRNA in the Vechur genotype. Environmental stress and heat tolerance were measured. Expression profiling indicated that ATP1A1 was differentially expressed in the phenotypically disparate cattle breeds. A molecular evolutionary genetic analysis revealed that the divergent origin of dwarf cattle was adaptive in response to heat stress and suggests the potential use of ATP1A1 as a marker for heat tolerance. Climate change is an imminent threat to livestock production. One adaptation strategy is selection for heat tolerance. While it is established that the ATP1A1 gene and its product play an important role in the response to many stressors, there has been no attempt to characterize the sequence or to perform expression profiling of the gene in production animals. We undertook a field experiment to compare the expression profiles of ATP1A1 in heat-tolerant Vechur and Kasaragod cattle (Bos taurus indicus) with the profile of a heat-susceptible crossbreed (B. t. taurus × B. t. indicus). The cattle were exposed to heat stress while on pasture in the hot summer season. The environmental stress was quantified using the temperature humidity index (THI), while the heat tolerance of each breed was assessed using a heat tolerance coefficient (HTC). The ATP1A1 mRNA of Vechur cattle was amplified from cDNA and sequenced. The HTC varied significantly between the breeds and with time-of-day (p < 0.01). The breed–time-of-day interaction was also significant (p < 0.01). The relative expression of ATP1A1 differed between heat-tolerant and heat-susceptible breeds (p = 0.02). The expression of ATP1A1 at 08:00, 10:00 and 12:00, and the breed–time-of-day interaction, were not significant. The nucleotide sequence of Vechur ATP1A1 showed 99% homology with the B. t. taurus sequence. The protein sequence showed 98% homology with B. t. taurus cattle and with B. grunniens (yak) and 97.7% homology with Ovis aries (sheep). A molecular clock analysis revealed evidence of divergent adaptive evolution of the ATP1A1 gene favoring climate resilience in Vechur cattle. These findings further our knowledge of the relationship between the ATP1A1 gene and heat tolerance in phenotypically incongruent animals. We propose that ATP1A1 could be used in marker assisted selection (MAS) for heat tolerance. [ABSTRACT FROM AUTHOR]