Mar 2024, Volume 19 Issue 3
    

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  • EDITORIAL
    Wenhua XIONG
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  • REVIEW
    Ivana MIRKOV, Dina TUCOVIC, Jelena KULAS, Anastasija MALESEVIC, Dragan KATARANOVSKI, Milena KATARANOVSKI, Aleksandra POPOV ALEKSANDROV
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    The importance of issues associated with urban/commensal rats and mice (property damage, management costs, and health risks) press upon research on these animals. While the demography of commensal rodents is mostly studied, the need for understanding factors influencing their natural morbidity/mortality is also stressed. In this respect, more attention is expected to be paid to immunity, the physiological mechanism of defense against host survival threats (pathogens, parasites, diseases). Commensal rats and mice carry numerous pathogens that evoke diverse immune responses. The state of immunity in commensal house mice is studied in great detail, owing to the use of laboratory strains in biomedical research. Because commensal rats are, compared to mice, carriers of more zoonotic agents, rats' immunity is studied mainly in that context. Some of these zoonotic agents cause chronic, asymptomatic infections, which justified studies of immunological mechanisms of pathogen tolerance versus clearance regulation in rats. Occurrence of some infections in specific tissues/organs pressed upon analysis of local/regional immune responses and/or immunopathology. A survey of immunological activity/responses in commensal rats is given in this review, with mention of existing data in commensal mice. It should throw some light on the factors relevant to their morbidity and lifespan, supplementing the knowledge of commensal rodent ecology.

  • ORIGINAL ARTICLE
    Qianqian SU, Yi CHEN, Hongxuan HE
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    Toll-like receptors (TLRs), the key sensor molecules in vertebrates, trigger the innate immunity and prime the adaptive immune system. The TLR family of rodents, the largest order of mammals, typically contains 13 TLR genes. However, a clear picture of the evolution of the rodent TLR family has not yet emerged and the TLR evolutionary patterns are unclear in rodent clades. Here, we analyzed the natural variation and the evolutionary processes acting on the TLR family in rodents at both the interspecific and population levels. Our results showed that rodent TLRs were dominated by purifying selection, but a series of positively selected sites (PSSs) primarily located in the ligand-binding domain was also identified. The numbers of PSSs differed among TLRs, and nonviral-sensing TLRs had more PSSs than those in viral-sensing TLRs. Gene-conversion events were found between TLR1 and TLR6 in most rodent species. Population genetic analyses showed that TLR2, TLR8, and TLR12 were under positive selection in Rattus norvegicus and R. tanezumi, whereas positive selection also acted on TLR5 and TLR9 in the former species, as well as TLR1 and TLR7 in the latter species. Moreover, we found that the proportion of polymorphisms with potentially functional change was much lower in viral-sensing TLRs than in nonviral-sensing TLRs in both of these rat species. Our findings revealed the first thorough insight into the evolution of the rodent TLR genetic variability and provided important novel insights into the evolutionary history of TLRs over long and short timescales.

  • ORIGINAL ARTICLE
    Sujatha MAYADUNNAGE, Hayley Jade STANNARD, Peter WEST, Julie M. OLD
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    There is currently limited information regarding the levels of infection and distribution of sarcoptic mange in the wombat population throughout Australia. We analyzed cases of sarcoptic mange in bare-nosed wombats reported into WomSAT, a website and mobile phone application where citizen scientists can upload sightings of wombats, burrows, and sarcoptic mange status. We used Maxent software to predict locations and the environmental factors associated with sarcoptic mange occurrence in bare-nosed wombats. A total of 1379 sarcoptic mange-infected and 3043 non-sarcoptic mange-infected wombats were reported by 674 and 841 citizen scientists, respectively. Of all the wombats reported to WomSAT from 2015 to 2019, 31.2% were infected with sarcoptic mange. Sarcoptic mange in bare-nosed wombats was reported in 502 suburbs across four states. New South Wales had the highest number of sarcoptic mange cases reported to WomSAT. There was no statistically significant seasonal variation of sarcoptic mange levels in bare-nosed wombats. The model showed that Euclidean distance to urban areas was the highest contributing factor for sarcoptic mange occurrence. As distance to urban areas decreased, the suitability for sarcoptic mange increased. Annual precipitation was the next contributing factor in the model, with higher rainfall of 400–700 mm correlating to an increase in sarcoptic mange occurrence. As the data collected to date have provided the largest-scale contemporary distribution of sarcoptic mange in wombats, data should continue to be collected by citizen scientists as it is an easy and low-cost method of collecting data over large areas. We suggest targeting the identified hotspot areas and more site-specific studies for studying and mitigating sarcoptic mange in bare-nosed wombats.

  • ORIGINAL ARTICLE
    Paulo MEJIA, Gustavo Lima URBIETA, Bruna da Silva XAVIER, Isaí Jorge de CASTRO, José Júlio DE TOLEDO, Gustavo GRACIOLLI, Lucio André VIANA DIAS, William Douglas CARVALHO
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    Bats are the second-most diverse group of mammals in the world, and bat flies are their main parasites. However, significant knowledge gaps remain regarding these antagonistic interactions, especially since diverse factors such as seasonality and host sex can affect their network structures. Here, we explore the influence of such factors by comparing species richness and composition of bat flies on host bats, as well as specialization and modularity of bat–bat fly interaction networks between seasons and adult host sexes. We captured bats and collected their ectoparasitic flies at 10 sampling sites in the savannahs of Amapá State, northeastern region of the Brazilian Amazon. Despite female bats being more parasitized and recording greater bat fly species richness in the wet season, neither relationship was statistically significant. The pooled network could be divided into 15 compartments with 54 links, and all subnetworks comprised >12 compartments. The total number of links ranged from 27 to 48 (for the dry and wet seasons, respectively), and female and male subnetworks had 44 and 41 links, respectively. Connectance values were very low for the pooled network and for all subnetworks. Our results revealed higher bat fly species richness and abundance in the wet season, whereas specialization and modularity were higher in the dry season. Moreover, the subnetwork for female bats displayed higher specialization and modularity than the male subnetwork. Therefore, both seasonality and host sex contribute in different ways to bat–bat fly network structure. Future studies should consider these factors when evaluating bat–bat fly interaction networks.

  • LETTER TO THE EDITOR
    João Pedro Rueda FURLAN, Micaela Santana RAMOS, Fábio Parra SELLERA, Irys Hany Lima GONZALEZ, Patrícia Locosque RAMOS, Eliana Guedes STEHLING
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    Enterobacterales and Pseudomonas aeruginosa have been colonizing or infecting wild hosts and antimicrobial-resistant strains are present in mammals and birds. Furthermore, international high-risk clones of multidrug-resistant Escherichia coli are identified and the implications of multidrug-resistant Gram-negative bacteria in zoo animals are discussed.

  • ESSAY
    Nubia E. MATTA, Wenhua XIONG
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  • REVIEW
    Tongtong GU, Jingyang HU, Li YU
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    Pangolins (Pholidota, Manidae) are classified as an evolutionarily distinct and globally endangered mammal due to their unique morphology (nail-like scales and a myrmecophagous diet) and being the victim of heavy poaching and worldwide trafficking. As such, pangolins serve as a textbook example for studying the special phenotypic evolutionary adaptations and conservation genetics of an endangered species. Recent years have demonstrated significant advancements in the fields of molecular genetics and genomics, which have translated to a series of important research achievements and breakthroughs concerning the evolution and conservation genetics of pangolins. This review comprehensively presents the hitherto advances in phylogeny, adaptive evolution, conservation genetics, and conservation genomics that are related to pangolins, which will provide an ample understanding of their diversity, molecular adaptation mechanisms, and evolutionary potentials. In addition, we highlight the priority of investigating species/population diversity among pangolins and suggest several avenues of research that are highly relevant for future pangolin conservation.

  • REVIEW
    Zheguang LIN, Siyi SHEN, Kang WANG, Ting JI
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    Honeybees are the most critical pollinators providing key ecosystem services that underpin crop production and sustainable agriculture. Amidst a backdrop of rapid global change, this eusocial insect encounters a succession of stressors during nesting, foraging, and pollination. Ectoparasitic mites, together with vectored viruses, have been recognized as central biotic threats to honeybee health, while the spread of invasive giant hornets and small hive beetles also increasingly threatens colonies worldwide. Cocktails of agrochemicals, including acaricides used for mite treatment, and other pollutants of the environment have been widely documented to affect bee health in various ways. Additionally, expanding urbanization, climate change, and agricultural intensification often result in the destruction or fragmentation of flower-rich bee habitats. The anthropogenic pressures exerted by beekeeping management practices affect the natural selection and evolution of honeybees, and colony translocations facilitate alien species invasion and disease transmission. In this review, the multiple biotic and abiotic threats and their interactions that potentially undermine bee colony health are discussed, while taking into consideration the sensitivity, large foraging area, dense network among related nestmates, and social behaviors of honeybees.

  • ORIGINAL ARTICLE
    Roman SHARNUUD, Eric I. AMECA
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    A significant research focus is placed on identifying animal species and areas at future risk to human-induced alterations of the environment and long-term changes in climatic conditions. Yet, the extent to which exposure to extreme climatic events and intense human pressure can increase the risk of harmful impacts on species remains poorly investigated. Focusing on terrestrial mammals in China, one of the world's megadiverse countries, we investigated patterns of contemporary exposure to floods and human pressures and determined their taxonomic representation and distribution across three major area-based conservation schemes, namely, national nature reserves (NNRs), priority areas for biodiversity conservation (PABCs), and key biodiversity areas (KBAs). Among the 440 species assessed with moderate or high exposure to floods, 327 (∼75%) also qualified as moderate or high in exposure to intense human pressure. These species mainly belong to the orders Chiroptera, Eulipotyphla, and Rodentia. Likewise, there were 305, 311, and 311 species with moderate or high exposure to flood and intense human pressure represented across NNRs, PABCs, and KBAs, respectively. Our findings support the prioritization of KBAs for expansion of site-based protection efforts such as NNRs in China, considering threats to species from exposure to adverse effects from both extreme climate and human pressure.

  • ORIGINAL ARTICLE
    Rui GUO, Guangwei MA, Xiaofei ZHAI, Haitao SHI, Jichao WANG
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    Red-eared sliders (Trachemys scripta elegans), as one of the 100 most threatening aliens, have stronger immunity than the native species in response to environmental stress. Blood cells are an important component of immunity in the body. However, the blood cell researches of turtle are still in the traditional blood cell classification and morphological structure observation. Furthermore, turtle granulocytes cannot be accurately identified using traditional methods. Single-cell RNA sequencing techniques have been successfully implemented to study cells based on the mRNA expression patterns of each cell. The present study profiled the transcriptomes of peripheral blood cells in red-eared sliders to construct a single-cell transcriptional landscape of the different cell types and explored environmental adaptation mechanism from the perspective of hematology. All 14 transcriptionally distinct clusters (platelets, erythrocytes1, erythrocytes2, CSF1R monocytes, POF1B monocytes, neutrophils, GATA2high basophils, GATA2low basophils, CD4 T cells, CD7 T cells, B cells, ACKR4 cells, serotriflin cells, and ficolin cells) were identified in the peripheral blood cells of the red-eared sliders. In particular, a subtype of erythrocytes (erythrocytes1) that expressed immune signals was identified. Peripheral blood cells were grouped into three lineages: platelet, erythroid/lymphoid, and myeloid cell lineages. Furthermore, based on differentiation trajectory and up-regulated gene expression, ACKR4 cells were newly identified as lymphocytes, and serotriflin and ficolin cells as granulocytes. The single-cell transcriptional atlas of the peripheral blood cells in red-eared sliders provided in the present study will offer a comprehensive transcriptome reference for the exploration of physiological and pathological hematology in this species.

  • ORIGINAL ARTICLE
    Mauricio HERNÁNDEZ, Stephanie HEREIRA-PACHECO, Antton ALBERDI, Aníbal H. DÍAZ DE LA VEGA-PÉREZ, Arturo ESTRADA-TORRES, Sergio ANCONA, Yendi E. NAVARRO-NOYA
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    Diet composition and its ecological drivers are rarely investigated in coexisting closely related species. We used a molecular approach to characterize the seasonal variation in diet composition in four spiny lizard species inhabiting a mountainous ecosystem. DNA metabarcoding revealed that the lizards Sceloporus aeneus, S. bicanthalis, S. grammicus, and S. spinosus mostly consumed arthropods of the orders Hemiptera, Araneae, Hymenoptera, and Coleoptera. The terrestrial lizards S. aeneus and S. bicanthalis mostly predated ants and spiders, whereas the arboreal–saxicolous S. grammicus and saxicolous S. spinosus largely consumed grasshoppers and leafhoppers. The taxonomic and phylogenetic diversity of the prey was higher during the dry season than the rainy season, likely because reduced prey availability in the dry season forced lizards to diversify their diets to meet their nutritional demands. Dietary and phylogenetic composition varied seasonally depending on the species, but only dietary composition varied with altitude. Seasonal dietary turnover was greater in S. spinosus than in S. bicanthalis, suggesting site-specific seasonal variability in prey availability; no other differences among species were observed. S. bicanthalis, which lives at the highest altitude in our study site, displayed interseasonal variation in diet breadth. Dietary differences were correlated with the species’ feeding strategies and elevational distribution, which likely contributed to the coexistence of these lizard species in the studied geographic area and beyond.

  • ORIGINAL ARTICLE
    Shaobin LI, Yuxin LIU, Xiaolong DU, Guopan LI, Wenbo LIAO
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    Amniotes differ substantially in absolute and relative brain size after controlling for allometry, and numerous hypotheses have been proposed to explain brain size evolution. Brain size is thought to correlate with processing capacity and the brain's ability to support complex manipulation such as nest-building skills. The increased complexity of nest structure is supposed to be a measure of an ability to manipulate nesting material into the required shape. The degree of nest-structure complexity is also supposed to be associated with body mass, partly because small species lose heat faster and delicate and insulated nests are more crucial for temperature control of eggs during incubation by small birds. Here, we conducted comparative analyses to test these hypotheses by investigating whether the complexity of species-typical nest structure can be explained by brain size and body mass (a covariate also to control for allometric effects on brain size) across 1353 bird species from 147 families. Consistent with these hypotheses, our results revealed that avian brain size increases as the complexity of the nest structure increases after controlling for a significant effect of body size, and also that a negative relationship exists between nest complexity and body mass.

  • ORIGINAL ARTICLE
    Ali AMER, Sierra SPEARS, Princeton L. VAUGHN, Cece COLWELL, Ethan H. LIVINGSTON, Wyatt MCQUEEN, Anna SCHILL, Dustin G. REICHARD, Eric J. GANGLOFF, Kinsey M. BROCK
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    Many species exhibit color polymorphisms which have distinct physiological and behavioral characteristics. However, the consistency of morph trait covariation patterns across species, time, and ecological contexts remains unclear. This trait covariation is especially relevant in the context of invasion biology and urban adaptation. Specifically, physiological traits pertaining to energy maintenance are crucial to fitness, given their immediate ties to individual reproduction, growth, and population establishment. We investigated the physiological traits of Podarcis muralis, a versatile color polymorphic species that thrives in urban environments (including invasive populations in Ohio, USA). We measured five physiological traits (plasma corticosterone and triglycerides, hematocrit, body condition, and field body temperature), which compose an integrated multivariate phenotype. We then tested variation among co-occurring color morphs in the context of establishment in an urban environment. We found that the traits describing physiological status and strategy shifted across the active season in a morph-dependent manner—the white and yellow morphs exhibited clearly different multivariate physiological phenotypes, characterized primarily by differences in plasma corticosterone. This suggests that morphs have different strategies in physiological regulation, the flexibility of which is crucial to urban adaptation. The white-yellow morph exhibited an intermediate phenotype, suggesting an intermediary energy maintenance strategy. Orange morphs also exhibited distinct phenotypes, but the low prevalence of this morph in our study populations precludes clear interpretation. Our work provides insight into how differences among stable polymorphisms exist across axes of the phenotype and how this variation may aid in establishment within novel environments.

  • ORIGINAL ARTICLE
    Lixin GONG, Huan WU, Zhiqiang WANG, Hui WU, Jiang FENG, Tinglei JIANG
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    Anti-predation strategies are critical to animal survival and are fundamental to deciphering predator–prey interactions. As an important defense strategy, sensory predator detection (such as through acoustic and visual cues) enables animals to assess predation risk and execute predator-avoidance behavior; however, there are limited studies on the anti-predation behavior of nocturnal animals. The prey of bats provides an excellent representative system for examining the anti-predation behavior of nocturnal animals. Here, we broadcasted different types of echolocation calls of the bird-eating bat Ia io to two wild passerine birds, namely, Zosterops japonicus and Sinosuthora webbiana, that are preyed upon by I. io, and presented the birds with individual bats under different light intensities. The results showed that both bird species were able to perceive the low-frequency audible portion of the bats’ echolocation calls; however, they did not exhibit escape responses to the acoustic stimuli. In the dark and under moonlit conditions, both bird species were unable to respond to active bats at close range and the birds only exhibited evasive flight behavior when bats approached or touched them. These results suggest that nocturnal passerine birds may not be able to use acoustic or visual cues to detect bats and adopt evasive maneuvers to avoid predation. This work suggests that bat predation pressure may not elicit primary predator-avoidance responses in nocturnal passerine birds. The results provide new insights into the anti-predation behavior of nocturnal animals.

  • ORIGINAL ARTICLE
    Vasily D. YAKUSHOV, Boris I. SHEFTEL
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    The dynamics of populations of small mammals of Central Siberia was analyzed. The studies were carried out at the Yenisei ecological station “Mirnoye” of the A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences. The time series analysis was performed by the wavelet transform using the statistical data processing language R. In the 20th century, the dynamics of the population of the community and some of its constituent species (Sorex araneus; S. caecutiens; S. isodon; S. tundrensis; S. minutus; Craseomys rufocanus; Clethrionomys rutilus; Microtus oeconomus; M. agrestis) were characterized by a 4-year periodicity. The type of dynamics changed to noncyclic by the nineties, but by 2022, four species (S. araneus, S. isodon, C. rutilus, and M. oeconomus) and the community as a whole showed a tendency toward recovery of population cycles. The remaining species were characterized by consistently low numbers with irregular low amplitude fluctuations.

  • ORIGINAL ARTICLE
    Kazım HALAÇLAR, Ayla SEVIM EROL, Tolga KÖROĞLU, Paul RUMMY, Tao DENG, Serdar MAYDA
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    The Çorakyerler fossil locality in Anatolia reveals unique faunal elements. This study introduces Hystrix kayae sp. nov., a new Late Miocene porcupine initially classified as Hystrix sp. Yavuz et al., 2018. This finding expands our knowledge of Late Miocene Anatolian porcupines, bringing the total number of known species to three. H. kayae sp. nov. is larger than Hystrix aryanensis and exhibits greater upper cheek tooth crown height. Its cheek tooth morphology differs from Hystrix depereti, and it possesses distinctive U-shaped choanae unlike Hystrix primigenia. The Çorakyerler locality may predate sites with H. aryanensis and H. primigenia but aligns temporally with Hystrix parvae localities. This study enhances our understanding of Late Miocene porcupine diversity in Anatolia, emphasizing the importance of Çorakyerler in unraveling the evolutionary history of these fascinating mammals.

  • ORIGINAL ARTICLE
    Shengnan YANG, Jiapeng QU, Ke TANG, Xinquan ZHAO, Huakun ZHOU, Junhua HU
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    The plateau environments are typically arid, cool, and high altitude, posing formidable challenges to wildlife survival due to resource scarcity and harsh conditions. Unraveling ecological adaptability in severe conditions requires a deeper understanding of the niche characteristics of plateau species. Trophic niche, which is a comprehensive indicator describing the energy acquisition strategy of animals, remains relatively understudied in plateau species. Here, by combining stable isotopes and morphological data, we quantified the trophic niches of two allopatric lizard species (Phrynocephalus vlangalii and P. erythrurus) that live in the hinterland of the Qinghai–Tibetan Plateau, and explored how their trophic niches correlate with morphological and environmental factors. While both trophic niche and morphological traits were similar between species, noteworthy distinctions were observed between male and female Phrynocephalus lizards. The morphological traits associated with predation (i.e. limb length and head size) and reproduction (i.e. abdomen length), annual mean temperature, and sex played influential roles in shifting trophic niches. These results imply that sexual dimorphism may facilitate inter-sex divergence in resource utilization, leading to trophic niche variations in the highland lizards. Furthermore, extreme environmental stress can constrain interspecific divergence in morphological and trophic traits. Our findings illustrate the dynamic variations of trophic niches in highland lizards, contributing to a more comprehensive understanding of the adaptation strategies employed by lizard species in plateau environments.

  • SHORT COMMUNICATION
    Artur GOLAWSKI, Iris CHARALAMBIDOU, Sylwia GOLAWSKA
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    Escape behavior is a common antipredator strategy among wild animals. Here, we investigated the effect of four factors on the vigilance behavior of the endemic Cyprus rock agama (Laudakia cypriaca). Flight initiation distance (FID, the minimum distance to which an observer can approach a lizard before it flees) was measured in relation to the type of location (tourist vs. nontourist area), the observer's starting distance, air temperature, and substrate temperature. We collected data for 39 agamas in tourist areas and 34 of these lizards in nontourist areas. As a whole, the mean starting distance was 10.5 m and the FID was 3.6 m. The average substrate temperature was 34.0°C and the average air temperature 29.6°C. Only the type of area affected the agamas’ escape decisions with FID being 1.8 m shorter in tourist areas than in nontourist areas (2.7 m vs. 4.5 m). This is probably due to the habituation of lizards to the presence of humans in the former areas. This study shows that tourism strongly affects the behavior of lizards, which may have consequences for the functioning of the population. Tourists can increase the safety of lizards by creating a human shield to deter predators. Once the tourist season is over, lizards may become more vulnerable to predators.