Local Adaptation of Bitter Taste and Ecological Speciation in a Wild Mammal

Abstract

Sensory systems are attractive evolutionary models to address how organisms adapt to local environments that can cause ecological speciation. However, tests of these evolutionary models have focused on visual, auditory, and olfactory senses. Here we show local adaptation of bitter taste receptor genes in two neighboring populations of a wild mammal—the blind mole rat Spalax galili—that show ecological speciation in divergent soil environments. We found that basalt-type bitter receptors showed higher response intensity and sensitivity compared with chalk-type ones using both genetic and cell-based functional analyses. Such functional changes could help animals adapted to basalt soil select plants with less bitterness from diverse local foods, whereas a weaker reception to bitter taste may allow consumption of a greater range of plants for animals inhabiting chalk soil with a scarcity of food supply. Our study shows divergent selection on food resources through local adaptation of bitter receptors, and suggests that taste plays an important yet underappreciated role in speciation.

Host diet shapes functionally differentiated gut microbiomes in sympatric speciation of blind mole rats in Upper Galilee, Israel

“…This particular phylum of bacteria is reported to be positively correlated with the fat intake of the host diet, and is significantly richer in populations with a high-fat diet than that of the malnutritional population ( Méndez-Salazar et al, 2018 ). In this study, the basalt mole rat population was mainly feeding on geophytes ( Jiao et al, 2021 ; Joyce et al, 2022 ), which have higher fat than that in Eryngium sp. roots from chalk; this is congruent with the functional enrichment pathway of fatty acid degradation and Glycerolipid metabolism ( Figure 3E ) in basalt population.…”

“…The ancestral chalk species is from Senonian, while the basalt species is from a volcanic eruption during the Quaternary, which is like basalt islands floating on chalk ocean ( Figure 1B ; Segev et al, 2002 ). When the volcano initially erupted about 1 million years ago and cooled down, new vegetation ( Hadid et al, 2013 ), food resources ( Figures 1C , 2C ), and ecological niches ( Figure 1B ) emerged, allowing animals to immigrate from the ancestral chalk to the new derivative symparic species on the basalt, forming the new species on the basalt ( Hadid et al, 2013 ; Nevo, 2013 ; Singaravelan et al, 2013 ; Li K. et al, 2015 ; Lövy et al, 2015 , 2017 , 2020 ; Li et al, 2016 , 2020a , b ; Šklíba et al, 2016 ; Jiao et al, 2021 ; Mukherjee et al, 2022 ; Nevo and Li, 2022 ; Figures 1A , 2C ). This provided us with an ideal model to further understand the complex interaction of the gut microbiome, the host, and its corresponding environment.…”

“…leaves; while the S. galili basalt mainly feed on geophytes, including Hordeum bulbosum, Bellevalia sp., Iris histrio, and a very small amount of Eryngium sp. (Jiao et al, 2021). The geophytes from the basalt are rich in protein and fat, while it is rich in cellulose in bushlets roots in chalk (Lövy et al, 2015(Lövy et al, , 2017.…”

“…The food resource diversity is much higher in basalt than in chalk ( Lövy et al, 2015 , 2017 ). There are more geophytes in basalt, whereas the bushlets of Sarcopoterium spinosum conquered the majority of the chalk soil ( Lövy et al, 2017 ; Jiao et al, 2021 ). The geophytes are more nutritious for the blind mole rats ( Mohammad and Alseekh, 2013 ), whereas those from the chalk feeding on primarily on roots may experience limited and low-quality food supply.…”

Functional Diversity and Evolution of Bitter Taste Receptors in Egg-Laying Mammals

“…β-glucosides include cyanogenic glucosides (CNglcs), highly deleterious and widely distributed biomolecules for feeding deterrents ( Beran et al 2019 ). While TAS2R16 of primates, rodents, and bats have sensitivity to β-glucosides ( Bufe et al 2002 ; Imai et al 2012 ; Jiao et al 2018 , 2021 ; Itoigawa et al 2019 ; Yang et al 2021 ), some primates which regularly feed on plants containing much CNglcs have TAS2R16 low sensitive to β-glucosides ( Itoigawa et al 2021 ). Therefore, β-glucoside detection would be important for survival in various mammals.…”