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. 2026 Feb 12;21(5):1460–1466. doi: 10.1111/1749-4877.70074

Retention of Sweet Taste in Sirenians Reflects Ecological Adaptation in Marine Mammals

Yingcan Li 1, Maoshu Wen 1, Yifan Feng 1, Huabin Zhao 1,✉
PMCID: PMC13574178  PMID: 41684201

Abstract

Taste perception is vital for animal survival. Among marine mammals, whales and pinnipeds have lost all sweet and umami taste receptor genes, whereas sirenians (manatees and dugongs) have retained them. The leading hypotheses for taste loss in marine mammals involve feeding behavior, dietary shifts, and high sodium concentrations. To characterize the evolution of sweet taste in sirenians, we analyzed the complete repertoire of sweet taste receptor genes (Tas1r2 and Tas1r3) and their coding sequences in 53 mammal species. Among marine mammals, only sirenians possessed intact sequences for both genes. Sequence analyses showed that both genes in sirenians are under strong purifying selection, comparable to that in most terrestrial mammals. Functional assays revealed that sirenians respond to natural sugars, but in species‐specific ways: Manatee receptors responded to both sucrose and fructose, whereas dugong receptors responded only to sucrose with lower sensitivity. Our findings provide the first evidence for the retention of natural sugar detection in sirenians and that this ability differs between species. Thus, sirenians are the only marine mammals known to have functional sweet taste, indicating that taste loss in other marine mammals is more likely linked to feeding behavior and diet rather than high sodium concentrations. The functional differences between manatees and dugongs likely reflect dietary divergence and ecological niche separation.

Keywords: diet, evolution, marine mammals, sirenians, taste receptor

This genetic study found that sirenians (manatees and dugongs) are the only marine mammals with conserved and functional sweet receptors. Moreover, functional differences in these receptors between manatees and dugongs align with their ecological divergences.

graphic file with name INZ2-21-1460-g001.webp

1. Introduction

The sense of taste allows animals to detect and distinguish foods by recognizing specific chemical compounds, playing a crucial role in survival and adaptation. In mammals, five basic tastes have been identified: sweet, umami, sour, salty, and bitter (Yarmolinsky et al. 2009). Sweet and umami tastes, mediated by the heterodimers Tas1r2+Tas1r3 and Tas1r1+Tas1r3, respectively, enable the detection of carbohydrates and amino acids (Zhao et al. 2003). Salty taste, mediated by the heterotrimer Scnn1a+Scnn1b+Scnn1g, facilitates electrolyte intake and maintains osmotic balance (Canessa et al. 1994). Bitter and sour tastes function primarily as protective mechanisms, deterring the ingestion of harmful or toxic substances via Tas2r and Otop1, respectively (Chandrashekar et al. 2000; Zhang et al. 2019).

The evolution of taste receptors is often closely linked to dietary preferences. Herbivorous and omnivorous mammals generally retain a larger repertoire of Tas2r genes, enabling them to avoid ingesting plant‐derived toxins (Policarpo et al. 2024). In contrast, many carnivorous mammals have lost Tas1r2 or the function of the sweet taste receptor due to the absence of carbohydrates in their diet, as seen in Carnivora (Jiang et al. 2012), insectivorous bats (Jiao et al. 2021), and pangolins (Li et al. 2024). Conversely, some species that shifted from carnivory to herbivory—such as the giant panda and red panda—have lost their umami taste through pseudogenization of Tas1r1 (Zhao et al. 2010; Hu et al. 2017).

Marine mammals exhibit the most pronounced contraction in taste receptor gene repertoires. They comprise three clades: cetaceans, pinnipeds, and sirenians. In cetaceans, genes associated with sweet, umami, sour, and most bitter tastes were pseudogenized in their common ancestor, leaving the salty receptor as the only potentially functional taste receptor (Feng et al. 2014). Similarly, pinnipeds have pseudogenized all Tas1r, resulting in the loss of sweet and umami taste (Jiang et al. 2012; Policarpo et al. 2024). A comparable pattern occurs in ocean‐adapted penguins, which have also lost Tas1r (Zhao et al. 2015). Anatomical studies show that these marine mammals have reduced taste bud structures: Cetaceans possess few lingual papillae (Iwasaki et al. 2019), while pinnipeds and sirenians have fewer papillae and taste buds than their terrestrial relatives (Levin and Pfeiffer 2002), suggesting a reduced reliance on taste. Proposed explanations include swallowing prey whole without mastication, high oceanic sodium levels that mask taste, and an exclusively carnivorous diet that reduces the functional necessity of taste (Feng et al. 2014).

Among marine mammals, sirenians are the only herbivores and likely possess the most developed sense of taste. Unlike other marine lineages, sirenians retain all three Tas1r (Policarpo et al. 2024). They also have six to seven Tas2r genes—fewer than their terrestrial relatives, elephants (which have 19), but still more than other marine mammals (Policarpo et al. 2024). Sirenians possess more taste buds than cetaceans and pinnipeds; for instance, the West Indian manatee has an average of 11,534 taste buds, a number comparable to that of rhesus monkeys (Barboza and Larkin 2020). The distribution of taste buds on the tongue also differs between manatees and dugongs (Marshall et al. 2022). Manatees have been reported to detect hormones and salinity, and distinguish among different foods (Best 1981). In aquatic environments, differentiating between olfaction and taste can be challenging; however, the loss of the vomeronasal organ and reduction in olfactory epithelium in sirenians suggest that taste may play a particularly important role in chemoreception (Marshall et al. 2022).

In this study, we address two questions. First, compared with other marine mammals, have sirenians retained sweet taste as a result of their herbivorous diet? Second, do manatees and dugongs differ in sweet taste perception due to differences in habitat and dietary breadth? To answer these questions, we analyzed the coding sequences of the sweet taste receptor genes Tas1r2 and Tas1r3 from 53 mammalian genomes. We also measured the functional properties of sweet taste receptors from the Indian manatee and dugong to assess whether sirenians can detect natural sugars and to evaluate the combined effects of marine adaptation and diet on sweet taste function.

2. Materials and Methods

2.1. Identification of Sweet Receptor Genes

We analyzed 53 high‐quality mammalian genomes from the National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov/, last accessed May 2024) to identify sweet receptor genes (Table S1). Genome assemblies were chosen based on assembly quality, phylogenetic representation, and an emphasis on including more marine mammal genomes. Following previous studies, human Tas1r2 and Tas1r3 protein sequences were used as queries in TBlastN searches (Altschul et al. 1990), with the best‐matching regions extended upstream and downstream, and coding sequences predicted using GeneWise (Madeira et al. 2024). Transmembrane structures were analyzed using TMHMM (Krogh et al. 2001). All sequences were classified as (1) intact genes, containing a 5′ start codon, a 3′ stop codon, a complete seven‐transmembrane domain structure, and an intact open reading frame (ORF); (2) pseudogenes, with an incomplete ORF caused by frameshifts or premature stop codons; or (3) partial genes, incomplete due to incomplete sequencing or poor genome assembly.

2.2. Phylogeny of Sweet Receptor Genes

Gene trees of intact Tas1r2 and Tas1r3 sequences were constructed using both a maximum likelihood approach with IQ‐TREE (Minh et al. 2020) and a Bayesian approach with Mrbayes 3.2.7 (Ronquist et al. 2012). The maximum likelihood analysis included 10 000 bootstrap replicates, while the Bayesian analysis ran for 2 000 000 generations. Multiple sequence alignments of intact Tas1r2 and Tas1r3 genes were performed based on amino acid sequences using MUSCLE (Edgar 2004). Pseudogenes were excluded to ensure reliable alignments, and mouse Vmn2r1 was used as the outgroup.

2.3. Evolutionary Analysis of Sweet Receptor Genes

Using the newly generated sequence alignments, we estimated the ratio (ω) of nonsynonymous substitutions to synonymous substitution rates with the codeml program in PAML version 4 (Yang 2007). Likelihood ratio tests were performed to compare alternative evolutionary models. The species tree used as input was sourced from previous studies (McGowen et al. 2020; Álvarez‐Carretero et al. 2022; Hao et al. 2024; Park et al. 2024; Wang et al. 2024; Yue et al. 2024).

2.4. Sweet Compounds

Two natural sugars, sucrose and fructose, were purchased from Sigma‐Aldrich for use in functional assays of sweet taste receptors. We did not include another natural sugar, glucose, because at high concentrations it can trigger nonspecific cellular responses in the heterologous expression system (Jiang et al. 2014). Following a previous study, sugars were diluted in DPBS (Thermo Fisher, pH 7.4) to a final concentration of 100 mM (Jiao et al. 2021).

2.5. Construction of Expression Vectors

We constructed expression vectors as previously described (Li et al. 2023; Xu et al. 2024). Briefly, the coding sequences of Tas1r2 and Tas1r3 from two sirenian species were chemically synthesized and inserted into the pcDNA3.1(+) vector using 5’‐EcoRI and 3’‐NotI restriction sites. The sequences were codon‐optimized, and a Kozak sequence was added at the 5’ end to enhance expression efficiency in Peakrapid cells. All plasmids were verified by Sanger sequencing.

2.6. Functional Assays of Sweet Receptors

Responses of sweet receptors to sugars were measured using calcium mobilization assays, following previously described protocols (Lu et al. 2021; Li et al. 2023). Briefly, PK cells cultured in OPTI medium with 7% FBS were seeded into 96‐well plates. At 70%–80% confluency, cells were transfected with sweet taste receptor constructs and Gα16‐gust44 using Lipofectamine 2000. After 2 days, intracellular calcium was labeled with Fluo‐4 and F‐127. Cells were then stimulated with sugar solutions, and corresponding fluorescence was recorded using the FlexStation 3 system (Molecular Devices). The FlexStation was set to measure fluorescence every 2 s for 200 s, with sugar solutions automatically added at 30 s. Receptor response was quantified as the change in fluorescence (ΔF/F), where ΔF is the difference between peak fluorescence (F max) after stimulation and the average baseline fluorescence (F).

3. Results

3.1. Collection of Sweet Receptor Genes in Mammals

To determine the evolutionary status of sweet taste receptors in marine mammals, we performed TBLASTN searches to identify Tas1r2 and Tas1r3 in 53 publicly available mammalian genome assemblies, including 18 marine mammals from three clades (Table S1). We identified 31 intact Tas1r2 genes, 22 pseudogenized Tas1r2 genes, 37 intact Tas1r3 genes, and 16 pseudogenized Tas1r3 genes (Figure 1; Dataset S1). Shared inactivating mutations indicate that in pinnipeds, Otariidae and Phocidae lost Tas1r2 and Tas1r3 independently, whereas in cetaceans, Tas1r3 was lost in their common ancestor, and Tas1r2 was lost independently in baleen and toothed whales (Figure S1). Gene trees were reconstructed using maximum likelihood and Bayesian methods to determine the phylogenetic relationships of the retrieved genes (Figure S2). No partial genes were detected, reflecting our use of high‐quality genome assemblies. For simplicity, mammalian sweet taste receptors were classified into three categories: (1) species with both genes intact, including 29 terrestrial mammals and two manatees; (2) species with only Tas1r2 lost, including six species manatees; (2) species with onger), tamanduas, koala, and Tasmanian devil; and (3) species with both Tas1r2 and Tas1r3 lost, including two groups of marine mammalscies withs and pinnipeds. Notably, both Tas1r2 and Tas1r3 are pseudogenized in all marine mammals except sirenians: the West Indian manatee (Trichechus manatus) and the dugong (Dugong dugon) (Figure 1).

FIGURE 1.

FIGURE 1

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Evolution of sweet taste receptor genes in mammals. The mammalian phylogeny with divergence times is based on previous studies (McGowen et al. 2020; Álvarez‐Carretero et al. 2022; Hao et al. 2024; Park et al. 2024). Dietary niches follow the published dataset (Wilman et al. 2014). The silhouettes of marine mammals were obtained from PhyloPic.

3.2. Evolutionary Analysis of Sweet Receptor Genes

To assess selective pressures acting on Tas1r2 and Tas1r3 in sirenians, we estimated the nonsynonymous‐to‐synonymous substitution rate ratio (ω = d N/d S) using a likelihood approach (Yang 2007). Under models A and E, which assume a single ω value for all branches, ω was estimated at 0.157 for Tas1r2 and 0.176 for Tas1r3; both values were significantly less than 1 (p < 0.0001 for both genes), indicating strong purifying selection (Table S2). We then fitted models D and H, allowing separate ω values for sirenians and terrestrial mammals, but found no significant improvement over models A and E (p = 0.609 and 0.113, respectively) (Table S2). These results suggest that sweet receptor genes in sirenians and terrestrial mammals have experienced similar levels of purifying selection.

3.3. Functional Assays of Sirenian Sweet Receptors

To determine whether sirenians have lost sweet taste perception, as observed in other marine mammals, we performed in vitro cell‐based functional assays for the two sirenian species: the West Indian manatee and the dugong (Figure 2). We obtained the first direct evidence of sweet taste perception in marine mammals: both sirenian sweet taste receptors responded to natural sugars (Figure 2A,B). Interestingly, the two species showed distinct response patterns. The manatee receptor exhibited strong responses to both sucrose (20.3%) and fructose (16.8%), whereas the dugong receptor responded weakly to sucrose (8.9%) and showed no response to fructose (Figure 2A,B). Dose–response curves confirmed sugar‐dependent activation in both species but revealed differences in sensitivity (Figure 2C,D). The manatee receptor detected as little as 12.5 mM of either sugar, while the dugong receptor required ≥25 mM sucrose, indicating lower sensitivity (Figure 2C,D).

FIGURE 2.

FIGURE 2

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Responses of sirenian sweet taste receptors to natural sugars. (A,B) Quantitative responses of sirenian sweet taste receptor to natural sugars (mean ± standard error of mean [SEM]; same letters indicate no significant difference [p > 0.05, one‐way ANOVA]). (C,D) Dose‐dependent responses for sirenian sweet taste receptors to natural sugars (* p < 0.05, one‐way ANOVA). (E,F) Quantitative responses of chimeric sirenian sweet taste receptors to natural sugars. MT2+DT3 denotes Tas1r2 from manatee combined with Tas1r3 from dugong; DT2+MT3 denotes the inverse combination: Tas1r2 from dugong combined with Tas1r3 from manatee.

Given these functional differences, we constructed chimeric receptors by combining Tas1r2 and Tas1r3 subunits from different species to identify the genetic basis of loss or reduction in function. Two chimeras were generated: MT2 + DT3 (Tas1r2 from manatee with Tas1r3 from dugong) and DT2 + MT3 (Tas1r2 from dugong with Tas1r3 from manatee) (Figure 2E,F). MT2 + DT3 displayed the same weak response pattern as the dugong receptor, indicating that mutations in Tas1r3 drive the loss of sweet taste in dugong. DT2 + MT3 showed stronger responses than the dugong receptor but remained weaker than the manatee's, suggesting that mutations in Tas1r2 also contribute to functional decline (Figure 2E,F). To test whether the sweet receptor experienced distinct selective pressures in the dugong and other mammals, we assigned ω1 to the dugong, ω2 to the manatee, and ω0 to other branches (Table S2). However, the models did not show a significant improvement over models D and I (p = 0.876 and 0.412, respectively). These results indicate that the sweet receptor in the dugong has not undergone a detectable change in selective pressure relative to the manatee. Thus, the loss of sweet taste function in the dugong is more likely attributable to a few critical amino acid substitutions that do not alter the overall d N/d S ratio.

4. Discussion

Why do sirenians still sense sweet? Previous studies have proposed three main hypotheses for the loss of taste in marine mammals: swallow‐feeding behavior, high sodium concentrations in seawater, and dietary shifts from plants to meat (Feng et al. 2014). Sirenians differ from other marine mammals in all three respects. As hindgut fermenters, they rely on mastication to rupture tough plant cell walls and improve digestive efficiency (Fritz et al. 2009). To accomplish this, manatees and dugongs have evolved specialized structures, dental pads, and keratinized palatal pads, respectively, that enable them to crush plant material effectively (Lanyon and Sanson 2006; Barboza and Kallaway 2024). Their diets further set them apart: Marine sirenians feed primarily on seagrasses, which are rich in starch and sucrose (Sogin et al. 2022; Ismael et al. 2023). Given their poor vision, reduced olfactory epithelium, and loss of the vomeronasal organ (Marshall et al. 2022), the ability to perceive sweetness may be especially important for identifying and selecting more nutritious seagrass species. Consistent with this idea, our functional assays show that sirenian sweet taste receptors respond strongly to natural sugars, indicating that the high sodium content of seawater exerts only a limited masking effect on their sweet perception. In contrast, the very different feeding behaviors and dietary profiles of other marine mammals may have driven the evolutionary loss of sweet taste in those lineages (Feng et al. 2014).

Although manatees and dugongs share a specialized herbivorous lifestyle, they differ markedly in sweet taste reception (Figure 2). Manatees exhibit strong responses to both sucrose and fructose, whereas dugongs respond weakly to sucrose and show no response to fructose, a pattern in which dietary breadth likely plays a key role. Dugongs are the only strictly marine herbivorous mammals, and their downturned snout prevents them from feeding at the surface, restricting them to bottom feeding and an almost exclusive reliance on seagrasses (André et al. 2005). When seagrass is scarce, they may supplement their diet with algae and invertebrates (Preen 1995). Seagrasses contain high starch concentrations in both leaves and below‐ground tissues (Aragones 1996), and can transfer sucrose to surrounding sediments via their roots (Policarpo et al. 2024). The carbohydrate content of seagrass influences dugong grazing behavior (De Iongh et al. 2007), suggesting that sweet taste may help optimize their energy intake.

In contrast to dugongs, all three manatee species regularly enter freshwater habitats, which broadens their ecological niches (Marsh et al. 2011). Manatees and dugongs also differ in the distribution of their taste buds (Yamasaki et al. 1980), and manatees’ flexible lips allow them to feed on surface algae, fallen mangrove leaves, and even low‐hanging vegetation (Castelblanco‐Martínez et al. 2009; Allen et al. 2018). In captivity, manatees are offered a variety of foods unavailable in the wild, further revealing their broader dietary flexibility compared with dugongs (Best 1981). All three manatee species have been reported to consume a variety of fruits (Takoukam Kamla et al. 2021), although records of the Indian manatee come from captive individuals (Harshaw et al. 2019). By contrast, no such fruit consumption has been reported for dugongs. The strong responses of manatee sweet taste receptors to both sucrose and fructose may underlie their broader diet and preference for fruits, contributing to the ecological niche divergence from dugongs, whose receptors respond weakly to sucrose and not at all to fructose.

Together, this study provides the first evidence that sirenians are the only marine mammals retaining the ability to detect natural sugars. Integrating previous findings on the relationship between taste and aquatic adaptation (Jiang et al. 2012; Feng et al. 2014), we show that herbivory and mastication have likely enabled sirenians to maintain sweet perception, with notable differences between species. This supports the view that taste loss in other marine mammals is more likely driven by feeding behavior and diet than by high sodium concentrations in seawater. Furthermore, the functional differences between manatees and dugongs appear to reflect dietary divergence and ecological niche separation.

Conflicts of Interest

The authors declare no conflicts of interest.

Supporting information

Dataset S1 Intact sequences of Tas1r2 and Tas1r3 identified or analyzed in this study.

INZ2-21-1460-s001.fasta (170.7KB, fasta)

Figure S1 Inactivating mutations in mammalian Tas1r2 and Tas1r3. The first or shared inactivating mutations are highlighted in red. Names of marine mammals are shown in bold. Numbers indicate the position of the first nucleotide in the alignment, corresponding to human Tas1r2 or Tas1r3.

INZ2-21-1460-s004.pdf (525.6KB, pdf)

Figure S2 Gene trees of mammalian Tas1r2 and Tas1r3. Two gene trees were constructed using the maximum likelihood (ML) method (A) and the Bayesian method (B). Sirenian genes are highlighted with red boxes.

INZ2-21-1460-s003.pdf (379.8KB, pdf)

Table S1 Genebank accession numbers for the genomes of 53 mammalian species used in this study.

INZ2-21-1460-s002.pdf (135.2KB, pdf)

Table S2 Selective pressure analysis on mammalian Tas1r2 and Tas1r3. p‐value less than 0.05 are highlighted in bold.

INZ2-21-1460-s006.pdf (166.8KB, pdf)

Supporting Information: inz270074‐sup‐0006‐SuppMat.pdf.

INZ2-21-1460-s005.pdf (143.1KB, pdf)

Acknowledgments

This work was supported in part by the National Natural Science Foundation of China (32270436) and the Fundamental Research Funds for the Central Universities (2042021kf0217).

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Dataset S1 Intact sequences of Tas1r2 and Tas1r3 identified or analyzed in this study.

INZ2-21-1460-s001.fasta (170.7KB, fasta)

Figure S1 Inactivating mutations in mammalian Tas1r2 and Tas1r3. The first or shared inactivating mutations are highlighted in red. Names of marine mammals are shown in bold. Numbers indicate the position of the first nucleotide in the alignment, corresponding to human Tas1r2 or Tas1r3.

INZ2-21-1460-s004.pdf (525.6KB, pdf)

Figure S2 Gene trees of mammalian Tas1r2 and Tas1r3. Two gene trees were constructed using the maximum likelihood (ML) method (A) and the Bayesian method (B). Sirenian genes are highlighted with red boxes.

INZ2-21-1460-s003.pdf (379.8KB, pdf)

Table S1 Genebank accession numbers for the genomes of 53 mammalian species used in this study.

INZ2-21-1460-s002.pdf (135.2KB, pdf)

Table S2 Selective pressure analysis on mammalian Tas1r2 and Tas1r3. p‐value less than 0.05 are highlighted in bold.

INZ2-21-1460-s006.pdf (166.8KB, pdf)

Supporting Information: inz270074‐sup‐0006‐SuppMat.pdf.

INZ2-21-1460-s005.pdf (143.1KB, pdf)

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