2024-06-20 2024, Volume 19 Issue 6

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  • ORIGINAL ARTICLE
    José MARTÍN , Gonzalo RODRÍGUEZ-RUIZ , Álvaro NAVARRO-CASTILLA , Isabel BARJA , Pilar LÓPEZ
    2024, 19(6): 1018-1033. https://doi.org/10.1111/1749-4877.12802

    Selecting a good mate is a decision with important fitness consequences. For this reason, mate choice has promoted the evolution of sexual ornaments signaling the quality of an individual. In fossorial animals, inhabiting visually restricted underground environments, chemical senses should be very important for mate choice. We examined whether sexual chemical signals (substrate scent marks) produced by males of the Iberian worm lizard,Blanus cinereus, a strictly fossorial blind amphisbaenian, provide information to females on morphological traits and health state. We administered corticosterone (CORT) to males simulating a continuous stressor affecting their health. Females preferred settling at sites scent-marked by males in comparison with similar sites with female scent or unmarked sites, but the attractiveness of males’ scent differed between individuals. Females preferred scent marks of larger/older males and with a higher immune response, while their body condition and CORT treatment were unrelated to female preferences. Chemical analyses showed that proportions of some compounds in precloacal secretions of males (used to produce scent marks) were correlated with the morphological (body size) and health state (immune response and body condition, but not CORT treatment) of these males. These results suggest that females may make site-selection decisions based on assessing the chemical characteristics of males’ scent marks, which were reliably related to some of the traits of the male that produced the scent. Therefore, females might use chemical senses to increase the opportunities to find and mate with males of high quality, coping with the restrictions of the subterranean environment.

  • ORIGINAL ARTICLE
    Xingzhi HAN , Baojun SUN , Qiong ZHANG , Liwei TENG , Fushun ZHANG , Zhensheng LIU
    2024, 19(6): 1034-1046. https://doi.org/10.1111/1749-4877.12784

    Climate warming poses a significant threat to species worldwide, particularly those inhabiting arid and semi-arid regions where extreme temperatures are increasingly prevalent. However, empirical studies investigating how moderate heat events affect the physiological processes of arid and semi-arid animals are largely scarce. To address this knowledge gap, we used an arid and semi-arid lizard species (Phrynocephalus przewalskii) as a study system. We manipulated thermal environments to simulate moderate heat events (43.5 ± 0.3°C during the heating period) for lizards and examined physiological and biochemical traits related to survival, metabolism, locomotion, oxidative stress, and telomere length. We found that the body condition and survival of the lizards were not significantly affected by moderate heat events, despite an increase in body temperature and a decrease in locomotion at high test temperatures were detected. Mechanistically, we found that the lizards exhibited down-regulated metabolic rates and enhanced activities of antioxidative enzymes, resulting in reduced oxidative damage and stable telomere length under moderate heat events. Based on these findings, which indicated a beneficial regulation of fitness by physiological and biochemical processes, we inferred that moderate heat events did not have a detrimental effect on the toad-headed agama,P. przewalskii. Overall, our research contributes to understanding the impacts of moderate heat events on arid and semi-arid species and highlights the adaptive responses and resilience exhibited by the toad-headed agama in the face of climate warming.

  • ORIGINAL ARTICLE
    Shahar DUBINER , Shai MEIRI , Eran LEVIN
    2024, 19(6): 1047-1056. https://doi.org/10.1111/1749-4877.12814

    In winter, many reptiles have a period of inactivity (“brumation”). During brumation there is no energetic intake, therefore there would be an advantage to reducing energetic expenditure. The size of energetically costly organs, a major determinant of metabolic rate, is known to be flexible in many tetrapods. Seasonal plasticity of organ size could serve as both an energy-saving mechanism and a source of nutrients for brumating reptiles. We studied a population of an invasive gecko,Tarentola annularis, to test for seasonal changes in activity, metabolic rate, and mass of various organs. The observed period of inactivity was December–February. Standard metabolic rates during the activity season were 1.85 times higher than in brumating individuals. This may be attributed to decreased organ mass during winter: heart mass decreased by 37%, stomach mass by 25%, and liver mass by 69%. Interestingly, testes mass increased by 100% during winter, likely in preparation for the breeding season, suggesting that males prioritize breeding over other functions upon return to activity. The size of the kidneys and lungs remained constant. Organ atrophy occurred only after geckos reduced their activity, so we hypothesize that organ mass changes in response to (rather than in anticipation of) cold winter temperatures and the associated fasting. Degradation of visceral organs can maintain energy demands in times of low supply, and catabolism of the protein from these organs can serve as a source of both energy and water during brumation. These findings bring us closer to a mechanistic understanding of reptiles’ physiological adaptations to environmental changes.

  • ORIGINAL ARTICLE
    Shufen JIANG , Changyi ZHANG , Xiao PAN , Kenneth B. STOREY , Wenyi ZHANG
    2024, 19(6): 1057-1075. https://doi.org/10.1111/1749-4877.12804

    Different responses or tolerance to thermal stress between invasive and native species can affect the outcome of interactions between climate change and biological invasion. However, knowledge about the physiological mechanisms that modulate the interspecific differences in thermal tolerance is limited. The present study analyzes the metabolic responses to thermal stress by the globally invasive turtle,Trachemys scripta elegans, as compared with two co-occurring native turtle species in China,Pelodiscus sinensis and Mauremys reevesii. Changes in metabolite contents and the expression or enzyme activities of genes involved in energy sensing, glucose metabolism, lipid metabolism, and tricarboxylic acid (TCA) cycle after exposure to gradient temperatures were assessed in turtle juveniles. Invasive and native turtles showed distinct metabolic responses to thermal stress. T. scripta elegans showed greater transcriptional regulation of energy sensors than the native turtles. Enhanced anaerobic metabolism was needed by all three species under extreme heat conditions, but phosphoenolpyruvate carboxykinase and lactate dehydrogenase in the invader showed stronger upregulation or stable responses than the native species, which showed inhibition by high temperatures. These contrasts were pronounced in the muscles of the three species. Regulation of lipid metabolism was observed in both T. scripta elegans and P. sinensis but not in M. reevesii under thermal stress. Thermal stress did not inhibit the TCA cycle in turtles. Different metabolic responses to thermal stress may contribute to interspecific differences in thermal tolerance. Overall, our study further suggested the potential role of physiological differences in mediating interactions between climate change and biological invasion.

  • ORIGINAL ARTICLE
    Jae-Uk SEOL , Jung Su PARK , Jae-Hong LIM , Hyeon Su HWANG , Eun-Bin KIM , Seob-Gu KIM , Jae-Il PARK , Ha-Cheol SUNG , Joon Heon KIM , Eung-Sam KIM
    2024, 19(6): 1076-1091. https://doi.org/10.1111/1749-4877.12821

    The tree frog is a prominent amphibian among terrestrial vertebrates known for its ability to adhere to various surfaces through the capillary forces of water in the microchannels between micropillars on its disc-shaped toe pads, a phenomenon known as wet adhesion. However, the secretion pattern of mucus on the attachment surface of living tree frog toe pads and the distribution of active mucus pores (AMPs) have not yet been fully elucidated. In this study, we utilized synchrotron X-ray micro-computed tomography and interference reflection microscopy to obtain the spatial distribution of the entire population of ventral mucus glands on the toe pads of living tree frogs and the real-time mucus secretion patterns from the ventral mucus pores on the contact surface under different environmental conditions. We observed that the number and secretion frequency of AMPs on the toe pad are regulated according to environmental conditions. Such dynamic mucus secretion on the tree frog’s toe pad could contribute to the understanding of capillary force regulation for wet adhesion and the development of adhesive surfaces by mimicking the mucus-secreting toe pad.

  • ORIGINAL ARTICLE
    Yuxin ZHANG , Handan XU , Chengjie TU , Runhua HAN , Jing LUO , Letian XU
    2024, 19(6): 1092-1104. https://doi.org/10.1111/1749-4877.12812

    Herbicides have demonstrated their impact on insect fitness by affecting their associated microbiota or altering the virulence of entomopathogenic fungi toward insects. However, limited research has explored the implications of herbicide stress on the intricate tripartite interaction among insects, associated bacterial communities, and entomopathogens. In this study, we initially demonstrated that associated bacteria confer a leaf beetle,Plagiodera versicolora, with the capability to resist the entomopathogenic fungus Aspergillus nomius infection, a capability sustained even under herbicide glyphosate stress. Further analysis of the associated microbiota revealed a significant alteration in abundance and composition due to glyphosate treatment. The dominant bacterium, post A. nomius infection or following a combination of glyphosate treatments, exhibited strong suppressive effects on fungal growth. Additionally, glyphosate markedly inhibited the pathogenic associated bacterium Pseudomonas though it inhibited P. versicolora’s immunity, ultimately enhancing the beetle’s tolerance to A. nomius. In summary, our findings suggest that the leaf beetle’s associated microbiota bestow an augmented resilience against the dual stressors of both the entomopathogen and glyphosate. These results provide insight into the effects of herbicide residues on interactions among insects, associated bacteria, and entomopathogenic fungi, holding significant implications for pest control and ecosystem assessment.

  • ORIGINAL ARTICLE
    Lijuan ZHAO , Chunxiao CHEN , Lewen WANG , Yan LIU , Fanglei GONG , Jingou WANG , Hong SUN , Dawei WANG , Zhenlong WANG
    2024, 19(6): 1105-1120. https://doi.org/10.1111/1749-4877.12818

    Photoperiod is a pivotal factor in affecting testicular function and spermatogenesis in seasonal-breeding animals. Mitophagy is essential for spermatogenesis, but its association with seasonal photoperiods has not been studied extensively. To explore this, we exposed male Brandt’s voles (Lasiopodomys brandtii) to long-photoperiod (LP, 16 h/day) and short-photoperiod (SP, 8 h/day) conditions from their embryonic stages. Our results indicated that testis weight, volume, and relative testes weight were all significantly increased in LP compared to SP. Additionally, blood testosterone levels were markedly higher in LP than SP. Histological examination revealed that seminiferous diameter and epithelium thickness were greater in LP, with an increased abundance of germ cell types and cell numbers compared to SP. RT-qPCR analysis showed that mitophagy-promoting genes, such as Pink1,Prkn,Tomm7,Mnf2,Lc3,Optn,Gabarap, and Nbr1 were all upregulated in LP. Fluorescence in situ hybridization indicated that Pink1 expression was present in spermatogonia in SP, while in LP,Pink1 expression extended to almost all germ cell types with significantly higher mean optical density. Prkn expression was found in all germ cell types in both LP and SP, with a significantly higher mean optical density of 10-week-old LP males. Transmission electron microscopy showed normal mitochondrial morphology with clear membranes in SP, while the LP group had reduced cristae in mitochondria and damaged mitochondria undergoing autophagy. This study suggests that mitophagy may be involved in the photoperiodic spermatogenesis in Brandt’s voles, providing insights into the role of photoperiod in seasonal reproduction in wild animals.

  • ORIGINAL ARTICLE
    Claudia ALLEGRINI , Carmi KORINE , Boris R. KRASNOV
    2024, 19(6): 1121-1134. https://doi.org/10.1111/1749-4877.12800

    Biotic and abiotic factors can act as filters for determining the species composition of biological communities. We aimed to identify abiotic factors driving the assembly of bat communities in Eastern Mediterranean pine plantations along a north–south climatic gradient, as they are crucial forest habitats for the assessment and conservation of these communities. We expected that bat communities are predominantly shaped by environmental filtering. We conducted acoustic sampling in 35 pine plantations in Israel and analyzed recordings for species identification. We used the ESLTP analysis, an extension of the three-table ordination (RLQ analysis), to explore relationships between environmental characteristics, species occurrences, and functional traits of species while accounting for phylogenetic relationships between species and spatial distribution of the communities. Communities showed phylogenetic and trait clustering. Climatic conditions and forest vegetation composition shaped communities of bats, affecting the distribution of traits related to foraging behaviors, vegetation clutter, and the ability of bats to maneuver in it. Maneuverable species were associated with the northern Mediterranean climatic zone, with a scarce cover of drought-tolerant small shrubs and grassland. Fast flyers were associated with the center-south semi-arid area, with abundant drought-tolerant small shrubs and grassland. These forces might have a predominant role in the assembly of these communities, presumably due to the stressful climatic conditions of the study area. The ESLTP approach can be extended to other taxa and environments to predict species responses to disturbance and environmental changes and give insights into environmental management.

  • ORIGINAL ARTICLE
    Baijie JIN , Xiangjun LI , Qingling ZHANG , Wen ZHOU , Yingyu LIU , Zimei DONG , Guangwen CHEN , Dezeng LIU
    2024, 19(6): 1135-1150. https://doi.org/10.1111/1749-4877.12780

    Microcystin-leucine arginine (MC-LR), a representative cyanobacterial toxin, poses an increasing and serious threat to aquatic ecosystems. Despite investigating its toxic effects in various organisms and cells, the toxicity to tissue regeneration and stem cells in vivo still needs to be explored. Planarians are ideal regeneration and toxicology research models and have profound implications in ecotoxicology evaluation. This study conducted a systemic toxicity evaluation of MC-LR, including morphological changes, growth, regeneration, and the underlying cellular and molecular changes after MC-LR exposure, which were investigated in planarians. The results showed that exposure to MC-LR led to time- and dose-dependent lethal morphological changes, tissue damage, degrowth, and delayed regeneration in planarians. Furthermore, MC-LR exposure disturbed the activities of antioxidants, including total superoxide dismutase, catalase, glutathione peroxidase, glutathione S-transferase, and total antioxidant capacity, leading to oxidative stress and DNA damage, and then reduced the number of dividing neoblasts and promoted apoptosis. The results demonstrated that oxidative stress and DNA damage induced by MC-LR exposure caused apoptosis. Excessive apoptosis and suppressed neoblast activity led to severe homeostasis imbalance. This study explores the underlying mechanism of MC-LR toxicity in planarians and provides a basis for the toxicity assessment of MC-LR to aquatic organisms and ecological risk evaluation.

  • ORIGINAL ARTICLE
    Wanxin LEI , Wei WEI , Dan PU , Shibu QUBI , Hong ZHOU , Mingsheng HONG , Junfeng TANG , Han HAN
    2024, 19(6): 1151-1162. https://doi.org/10.1111/1749-4877.12765

    Trophic niche is the result of the long-term evolution of species and can reflect the pressures they experience in habitats. The whole-genome sequencing of giant pandas (Ailuropoda melanoleuca) has indicated that populations distributed in Qinling (QIN) and non-QIN probably diverged 300 ky ago. Although many studies regarding foraging strategy, habitat preference, and niche partition have been conducted on these populations, there is still a lack of precise quantification of trophic niches. Here, we calculated and compared isotopic trophic niche widths of giant pandas from Sichuan (SC) and QIN populations by measuring carbon and nitrogen isotopes of their hairs; combined with data from sympatric mammals, we explored the relative trophic positions of giant pandas in the ecosystem, respectively. The Stable Isotope Bayesian Ellipses in R (SIBER) model results showed the trophic niche width of QIN pandas was 3.44‰2, which was significantly bigger than those of the SC population (2.03‰2), with an overlapping about 1.45‰2; and they both occupied a unique position in the context, almost one trophic level lower than herbivores. Then, we determined the isotopic ratios of the main foods from the habitats of these pandas; the results suggested that the isotopic difference between bamboo shoots and other parts plus the various feeding selections of pandas on them accounted for pandas’ trophic niche widths. We considered the higher nutrition availability and digestible food resources giving QIN pandas a wider trophic niche than pandas from SC. This conclusion provides a new insight into the resource use and trophic ecology of giant pandas and is important to develop refined management plans for the two populations.

  • ORIGINAL ARTICLE
    Boris R. KRASNOV , Georgy I. SHENBROT , Irina S. KHOKHLOVA , M. Fernanda LÓPEZ BERRIZBEITIA , Sonja MATTHEE , Juliana P. SANCHEZ , Luther VAN DER MESCHT
    2024, 19(6): 1163-1180. https://doi.org/10.1111/1749-4877.12799

    We studied spatial variation in the effects of environment and network size on species positions and roles in multiple flea–mammal networks from four biogeographic realms. We asked whether species positions (measured as species strength [SS], the degree of interaction specialization [d’], and the eigenvector centrality [C]) or the roles of fleas and their hosts in the interaction networks: (a) are repeatable/conserved within a flea or a host species; (b) vary in dependence on environmental variables and/or network size; and (c) the effects of environment and network size on species positions or roles in the networks depend on species traits. The repeatability analysis of species position indices for 441 flea and 429 host species, occurring in at least two networks, demonstrated that the repeatability of SS,d’, and C within a species was significant, although not especially high, suggesting that the indices’ values were affected by local factors. The majority of flea and host species in the majority of networks demonstrated a peripheral role. A value of at least one index of species position was significantly affected by environmental variables or network size in 41 and 36, respectively, of the 52 flea and 52 host species that occurred in multiple networks. In both fleas and hosts, the occurrence of the significant effect of environment or network size on at least one index of species position, but not on a species’ role in a network, was associated with some species traits.

  • ORIGINAL ARTICLE
    Pengbo LIU , Guichang LI , Ning ZHAO , Qiyong LIU , Xiaobo LIU , Xiuping SONG , Xinfei SHI , Xinchang LUN , Lu ZHANG , Jun WANG , Liang LU
    2024, 19(6): 1181-1198. https://doi.org/10.1111/1749-4877.12791

    Parasite-mediated selection is widely believed to play a crucial role in maintaining the diversity of the major histocompatibility complex (MHC) genes, which is thought to be maintained through heterozygote advantage, rare-allele advantage, and fluctuating selection. However, the relationship between parasite pressure and MHC diversity has yielded inconsistent findings. These inconsistencies may arise from the influence of environmental factors and individual variations in traits on host–parasite interactions. To address these issues, our study extensively investigated populations of striped hamsters inhabiting regions characterized by environmental heterogeneity. The primary objective was to examine the universality of parasite-mediated selection mechanisms. Our observations revealed the presence of multiple parasite infections, accompanied by spatial and temporal variations in parasite communities and infection patterns among individual hamsters. Specifically, the temperature was found to influence all four parasite indices, while the presence of gamasid mites and parasite richness decreased with increasing precipitation. We also noted significant seasonal variation in parasite dynamics. Moreover, a significant sexual dimorphism was observed with males exhibiting a considerably higher parasite burden compared to their female counterparts. Lastly, we identified the maintenance of MHC polymorphism in striped hamsters as being driven by the heterozygote advantage and fluctuating selection mechanisms. This study underscores the significance of ecological processes in comprehending host–parasite systems and highlights the necessity of considering environmental factors and individual traits when elucidating the mechanisms underlying MHC diversity mediated by parasites.

  • ORIGINAL ARTICLE
    Chuang ZHOU , Xiaofeng ZHENG , Kexin PENG , Kaize FENG , Bisong YUE , Yongjie WU
    2024, 19(6): 1199-1210. https://doi.org/10.1111/1749-4877.12795

    The kiang (Equus kiang) can only be observed in the Qinghai–Tibet Plateau (QTP). The kiang displayed excellent athletic performance in the high-altitude environment, which attracted wide interest in the investigation of the potential adaptive mechanisms to the extreme environment. Here, we assembled a chromosome-level genome of the kiang based on Hi-C sequencing technology. A total of 324.14 Gb clean data were generated, and the chromosome-level genome with 26 chromosomes (25 + X) and scaffold N50 of 101.77 Mb was obtained for the kiang. The genomic synteny analysis revealed large-scale chromosomal rearrangement during the evolution process of Equus species. Phylogenetic and divergence analyses revealed that the kiang was the sister branch to the ass and diverged from a common ancestor at approximately 13.5 Mya. The expanded gene families were mainly related to the hypoxia response, metabolism, and immunity. The kiang suffered a significant loss of olfaction-related genes, which might indicate decreased olfactory sensibility. Positively selected genes (PSGs) detected in the kiang were mainly associated with hypoxia response. Especially, there were two species-specific missense amino acid mutations in the PSG STAT3 annotated in the hypoxia-inducible factor 1 signal pathway, which may play an important role in the high-altitude adaptation of the kiang. Moreover, structure variations in the kiang genome were also identified, which possibly contributed to the high-altitude adaptation of the kiang. Comparative analysis revealed a lot of species-specific insertions and deletions in the kiang genome, such as PIK3CB and AKT with 3258 and 189 bp insertions in the intron region, respectively, possibly affecting the expression and regulation of hypoxia-related downstream pathways. This study provided valuable genomic resources, and our findings help a better understanding of the underlying adaptive strategies to the high-altitude environment in the kiang.

  • ORIGINAL ARTICLE
    Ashley M. DUNGAN , Jessica L. THOMAS
    2024, 19(6): 1211-1223. https://doi.org/10.1111/1749-4877.12865

    The duck-billed platypus (Ornithorhynchus anatinus) is currently listed as near-threatened. A key part of the conservation strategy for this species is its captive maintenance; however, captive animals often have dysbiotic gut bacterial microbiomes. Here, for the first time, we characterize the gut microbiome of wild platypus via fecal samples using high-throughput sequencing of the bacterial 16S rRNA gene and identify microbial biomarkers of captivity in this species. At the phylum level, Firmicutes (50.4%) predominated among all platypuses, followed by Proteobacteria (28.7%), Fusobacteria (13.4%), and Bacteroidota (6.9%), with 21 “core” bacteria identified. Captive individuals did not differ in their microbial α-diversity compared to wild platypus but had significantly different community composition (β-diversity) and exhibited higher abundances of Enterococcus, which are potential pathogenic bacteria. Four taxa were identified as biomarkers of wild platypus, including Rickettsiella,Epulopiscium,Clostridium, and Cetobacterium. This contrast in gut microbiome composition between wild and captive platypus is an essential insight for guiding conservation management, as the rewilding of captive animal microbiomes is a new and emerging tool to improve captive animal health, maximize captive breeding efforts, and give reintroduced or translocated animals the best chance of survival.

  • COMMENTARY
    Hao WANG , Hao ZHENG
    2024, 19(6): 1224-1226. https://doi.org/10.1111/1749-4877.12877
  • COMMENTARY
    Jiameng LI , Yinzi YE , Weiguo DU , Shilong YANG
    2024, 19(6): 1227-1228. https://doi.org/10.1111/1749-4877.12887
  • COMMENTARY
    Jing WEI , Yuxin ZHANG , Letian XU
    2024, 19(6): 1229-1232. https://doi.org/10.1111/1749-4877.12867
  • COMMENTARY
    Xiaoling LIANG , Weimin KUANG
    2024, 19(6): 1233-1235. https://doi.org/10.1111/1749-4877.12891