2025-05-20 2025, Volume 20 Issue 3

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  • REVIEW
    Zhuoqing LI , Meijie YANG , Cong ZHOU , Pu SHI , Pengpeng HU , Bin LIANG , Qingtian JIANG , Lili ZHANG , Xiaoyan LIU , Changping LAI , Tao ZHANG , Hao SONG

    The intricate process of shell biomineralization in marine molluscs is governed by a complex interplay of regulatory elements, encompassing secretomes, transporters, and noncoding RNA. This review delves into recent advancements in understanding these regulatory mechanisms, emphasizing their significance in elucidating the functions and evolutionary dynamics of the molluscan shell biomineralization process. Central to this intricate orchestration are secretomes with diverse functional domains, selectively exported to the extrapallial space, which directly regulate crystal growth and morphology. Transporters are crucial for substrate transportation in the calcification and maintenance of cellular homeostasis. Beyond proteins and transporters, noncoding RNA molecules are integral components influencing shell biomineralization. This review underscores the nonnegligible roles played by these genetic elements at the molecular level. To comprehend the complexity of biomineralization in mollusc, we explore the origin and evolutionary history of regulatory elements, primarily secretomes. While some elements have recently evolved, others are ancient genes that have been co-opted into the biomineralization toolkit. These elements undergo structural and functional evolution through rapidly evolving repetitive low-complexity domains and domain gain/loss/rearrangements, ultimately shaping a distinctive set of secretomes characterized by both conserved features and evolutionary innovations. This comprehensive review enhances our understanding of molluscan biomineralization at the molecular and genetic levels.

  • REVIEW
    Wei ZHANG , Lukasz L. STELINSKI , Amr MOHAMED , Guangmin WANG , Gianluca TETTAMANTI , Moxian CHEN , Mingsheng HONG , Ella Z. DALY , Jan BRUIN , David RENAULT , Nemat O. KEYHANI , Qi ZHAO

    Agricultural ecosystem formation and evolution depend on interactions and communication between multiple organisms. Within this context, communication occurs between microbes, plants, and insects, often involving the release and perception of a wide range of chemical cues. Unraveling how this information is coded and interpreted is critical to expanding our understanding of how agricultural ecosystems function in terms of competition and cooperation. Investigations examining dual interactions (e.g. plant–microbe, insect–microbe, and insect–plant) have resolved some basic components of this communication. However, there is a need for systematically examining multitrophic interactions that occur simultaneously between microorganisms, insects, and plants. A more thorough understanding of these multitrophic interactions has been made possible by recent advancements in the study of such ecological interactions, which are based on a variety of contemporary technologies such as artificial intelligence sensors, multi-omics, metabarcoding, and others. Frequently, these developments have led to the discovery of startling examples of each member manipulating the other. Here, we review recent advances in the understanding of bottom-up chemical communication between microorganisms, plants, and insects, and their consequences. We discuss the components of these “chemo-languages” and how they modify outcomes of multi-species interactions across trophic levels. Further, we suggest prospects for translating the current basic understanding of multitrophic interactions into strategies that could be applied in agricultural ecosystems to increase food safety and security.

  • ORIGINAL ARTICLE
    Ignasi FERNÁNDEZ-CABELLO , Marc FRANCH , Marc VILELLA , Nerea FERNANDEZ-ARRIETA , Marc ROTA , Ariadna SANGLAS , Eric BAQUÉ-DÍAZ , Marc GALLARDET , Pau FEDERICO , Albert PERIS , Eric SERRATOSA , Joan REAL , Ferran SAYOL , Roger PUIG-GIRONÈS

    Mammal species globally exhibit distribution patterns conditioned by environmental conditions and human impact. The Mediterranean basin provides an ideal system to study these effects due to its diverse climate, and habitat conditions. In this work, we aim to assess the impact of landscape heterogeneity and anthropization degree on terrestrial mammal diversity in this region. Accordingly, we deployed over 300 camera traps across 28 sites for 3 months. Detected mammal species (weighing more than 1kg) were classified as domestic carnivores, domestic ungulates, wild carnivores, wild ungulates, lagomorphs, and large rodents. Alpha and beta diversity were calculated for each group and all wild mammals. Simple linear regressions and multimodal analysis were conducted between mammal diversities and climate, environmental conditions, landscape heterogeneity, and anthropization degree variables. Redundancy analyses were performed to identify variables and species determining the mammalian community composition. Indexes measuring landscape heterogeneity, anthropization degree, and its 30-year change did not correlate with mammal diversity. However, the difference in elevation within sites and domestic carnivore abundance showed a significant positive correlation with some of the diversity indexes. Nonetheless, rainfall and mean elevation factors generally showed the highest correlation with mammal diversity. Instead, a few influential species, including generalists and open-habitat specialists, highlighted the importance of conserving open areas, as well as the importance of the Pyrenees region as a key habitat for certain species. Therefore, climatic variables emerged as the key determinants of mammal diversity, highlighting climate change as a potential threat to mammal diversity in this area.

  • ORIGINAL ARTICLE
    Dongyi WU , Pingshin LEE , Hongman CHEN , Fang YAN , Jiayue HUANG , Yanhong HE , Ruiyao WU , Zhiyong YUAN

    Environmental DNA (eDNA) metabarcoding has emerged as a powerful, non-invasive tool for biodiversity assessments. However, the accuracy and limitations of these assessment techniques are highly dependent on the choice of primer pairs being used. Although several primer sets have been used in eDNA metabarcoding studies of amphibians, there are few comparisons of their reliability and efficiency. Here, we employed lab- and field-tested sets of publicly available and de novo-designed primers in amplifying 83 species of amphibian from all three orders (Anura, Caudata, and Gymnophiona) and 13 families present in China to evaluate the versatility and specificity of these primers sets in amphibian eDNA metabarcoding studies. Three pairs of primers were highly effective, as they could successfully amplify all the major clades of Chinese amphibians in our study. A few non-amphibian taxa were also amplified by these primers, which implies that further optimization of amphibian-specific primers is still needed. The simultaneous use of three primer sets can completely cover all the species obtained by conventional survey methods and has even effectively distinguished quite a number of species (n = 20) in the Wenshan National Nature Reserve. No single primer set could individually detect all of the species from the studied region, indicating that multiple primers might be necessary for a comprehensive survey of Chinese amphibians. Besides, seasonal variations in amphibian species composition were also revealed by eDNA metabarcoding, which was consistent with traditional survey methods. These results indicate that eDNA metabarcoding has the potential to be a powerful tool for studying spatial and temporal community changes in amphibian species richness.

  • ORIGINAL ARTICLE
    Siqi WANG , Wenhao LI , Jiaqi ZHANG , Zexu LUO , Yiming LI

    Invasive alien species are a major driver of biodiversity loss. Currently, the process of biological invasions is experiencing a constant acceleration, foreshadowing a future increase in the threat posed by invasive alien species to global biodiversity. Therefore, it is necessary to assess the impact risks of invasive alien species and related factors. Here, we constructed a dataset of negative environmental impact events to evaluate the impact risks of alien species. We collected information on 1071 established alien terrestrial vertebrates and then gathered negative environmental impacts for 108 of those species. Generalized linear mixed-effects model and phylogenetic generalized least-squares regression model were used to examine the characteristic (including life-history traits, characteristics related to distribution, and introduction event characteristics) correlates of species’ impact risks at the global scale for 108 established alien terrestrial vertebrates (mammals, birds, reptiles and amphibians). Our results showed that a total of 3158 negative environmental impacts were reported for 108 harmful species across 71 countries worldwide. Factors associated with impact risks varied slightly among taxa, but alien range size, habitat breadth, origin location, and domestication were significantly correlated with impact risks. Our study aims to identify the characteristics of alien species with high-impact risks to facilitate urgent assessment of alien species and to protect the local ecological environment and biodiversity.

  • ORIGINAL ARTICLE
    Yongli DING , Ming ZOU , Baocheng GUO

    Scale morphology represents a fundamental feature of fish and a key evolutionary trait underlying fish diversification. Despite frequent and recurrent scale loss throughout fish diversification, comprehensive genome-wide analyses of the genomic signatures associated with scale loss in divergent fish lineages remain scarce. In the current study, we investigated genome-wide signatures, specifically convergent protein-coding gene loss, amino acid substitutions, and cis-regulatory sequence changes, associated with recurrent scale loss in two divergent Cypriniformes lineages based on large-scale genomic, transcriptomic, and epigenetic data. Results demonstrated convergent changes in many genes related to scale formation in divergent scaleless fish lineages, including loss of P/Q-rich scpp genes (e.g. scpp6 and scpp7), accelerated evolution of non-coding elements adjacent to the fgf and fgfr genes, and convergent amino acid changes in genes (e.g. snap29) under relaxed selection. Collectively, these findings highlight the existence of a shared genetic architecture underlying recurrent scale loss in divergent fish lineages, suggesting that evolutionary outcomes may be genetically repeatable and predictable in the convergence of scale loss in fish.

  • ORIGINAL ARTICLE
    Piotr JADWISZCZAK , Ashley KRÜGER , Thomas MÖRS

    Penguin tarsometatarsi are shortened and flattened, and studies devoted to the internal characteristics of these composite bones are very limited. Therefore, we present here a comprehensive, x-ray-microscopy-based analysis based on tarsometatarsi of Eocene stem Sphenisciformes from Seymour Island (Antarctic Peninsula) as well as recent Aptenodytes forsteri, A. patagonicus, and Pygoscelis adeliae penguins. Our study focuses on four aspects: size variability of the medullary cavities, vascularization patterns with emphasis on diaphyseal vessels, cross-sectional anisotropy, and diaphyseal resistance to bending forces. Small-sized Eocene penguins (Delphinornis and Marambiornopsis) show well-developed tarsometatarsal medullary cavities, whereas the cavities of “giant” early Sphenisciformes are either smaller (Palaeeudyptes) or show a conspicuous intermetatarsal size gradient (Anthropornis). Extant penguins exhibit a decrease in cavity dimensions as their body size increases. Distributional tendencies of primary diaphyseal nutrient foramina are quite similar in the smaller Delphinornis, Marambiornopsis, and extant Pygoscelis on one side and in Palaeeudyptes and extant Aptenodytes on the other. Anthropornis shows a unique, plesiomorphic pattern with a prevalence of plantar blood supply to the metatarsals. The diaphyseal nutrient canals diverge in orientation, some obliquely away from the proximal part, others with disparate trajectories. Cross-sectional anisotropy along the tarsometatarsal shaft generally appears to be rather low. Clustering of coherency curves along certain tarsometatarsal segments may reflect a selection process that exerts a significant influence within biomechanically crucial sections. Diaphyseal resistance to mediolateral bending forces is explicitly more efficient in extant penguins than in Eocene Sphenisciformes. This can be interpreted as an adaptation to the waddling gait of extant penguins.

  • ORIGINAL ARTICLE
    Ruidong CAO , Mingyu ZHANG , Yi CHEN , Guanmei HOU , Quansheng LIU , Jianxu ZHANG , Yaohua ZHANG

    Rattus species are thought to live only at altitudes less than 2500 m, but the Asian house rat (R. tanezumi) (RT) has recently expanded to altitudes greater than 3500 m in China. Other Rattus species, especially brown rats (R. norvegicus) (RN), still reach only low altitudes on the Tibetan Plateau. Comparative genomics revealed the positive selection of hypoxia-inducible transcription factors 1 and 2 (HIFs) in RT, with the rapid evolution of HIF pathway genes in RT and Mus musculus (MM) but not RN or R. rattus. Population genomics revealed that genes associated with energy metabolism and oxygen transport were positively selected in RT compared with the other four Rattus species, and two specific substitutions (arginine 31 serine and leucine 33 methionine) were identified in the hemoglobin subunit beta (HBB) in RT. The above results suggested that RT possesses unique genetic adaptations to hypoxia, which was further confirmed by behavioral experiments on RT and RN. Normobaric hypoxia significantly reduced locomotion in RN but not in RT. Moreover, through intraspecific transcriptome analysis, the expression of Hbb and genes related to angiogenesis, oxygen transport, and glycolysis was upregulated, and the expression of genes associated with immunological functions in the liver, lungs, and/or sperm was downregulated in RT compared to those in RN. Interspecific transcriptome analysis further revealed that HIF-1α plays a role in modulating the hypoxic adaptation of RT rather than RN. Our work provides genomic, behavioral, and physiological insights into why RT, but not other Rattus species, could invade the Tibetan Plateau.

  • ORIGINAL ARTICLE
    Zaiwei WANG , Amy MARTIN , Dianne BRUNTON , Cyril C. GRUETER , Jiapeng QU , Jin-Sheng HE , Weihong JI , Zhibiao NAN

    Grassland degradation is challenging the health of grassland ecosystems globally and causing biodiversity decline. Previous studies have demonstrated the impact of grassland degradation on the abundance and behavior of small mammals. Little is known about how it affects the genetic structure of gregarious mammals in the wild. This study explores the effects of grassland degradation on the genetic structure of a small burrowing mammal, plateau pika (Ochotona curzoniae). We used nine microsatellite loci to analyze the genetic diversity and genetic differentiation between colonies and genetic relatedness between individuals within the colony. We found that pikas in severely degraded grasslands had a significantly higher genetic diversity within colonies, a higher level of gene flow between colonies, and a lower genetic differentiation between colonies compared to pikas in less degraded grasslands. Individuals within colonies had a significantly lower genetic relatedness in severely degraded grasslands than in less degraded grasslands. This study has provided potential evidence of a significant impact of grassland degradation on the genetic structure of pikas, which has caused a breakdown of their kin-selected colony structure.

  • ORIGINAL ARTICLE
    Gary VOELKER , Guinevere O.U. WOGAN , Jerry W. HUNTLEY , Potiphar M. KALIBA , Dawie H. DE SWARDT , Rauri C. K. BOWIE

    Avian species diversity in Southern Africa is remarkably high, yet the mechanisms responsible for that diversity are poorly understood. While this is particularly true with respect to species endemic to the subregion, it is unclear as to how more broadly distributed African species may have colonized southern Africa. One process that may in part account for the high bird species diversity in southern Africa is a “species pump” model, wherein the region was repeatedly colonized by lineages from areas further north: a pattern related to climate cycling and the eastern African arid corridor. Once occupying southern Africa, with its many varied biomes, it is possible that climate cycling further affected lineages by generating genetic diversity in multiple refugia, a pattern recently shown for several southern African bird species. Here, we used mtDNA to address these questions in a widespread, sedentary habitat generalist bird species, the familiar chat (Oenanthe familiaris). The phylogenetic structure suggests a north-to-south colonization pattern, supporting the “species pump” model. Haplotype diversity was partitioned into two distinct clusters: southern Africa and Malawi (East Africa). Southern African haplotypes were not geographically partitioned, and we hypothesize that this pattern has arisen because this species is a habitat generalist, and as such resilient to habitat-altering climate perturbations. Based on our phylogenetic results, we discuss the validity of currently recognized subspecies.

  • ORIGINAL ARTICLE
    Kang AN , Baohui YAO , Yuchen TAN , Yukun KANG , Zhicheng WANG , Junhu SU

    Plateau zokor (Eospalax baileyi) is a subterranean rodent and seasonal breeder. During the non-breeding season, the testicles regress, leading to the arrest of spermatogenesis and loss of fertility. The identification of the specific germ cell type at which spermatogenesis is arrested, as well as potential regulatory factors during the non-breeding season, is important for understanding seasonal spermatogenesis in subterranean species. This study analyzed genes in spermatocytes of plateau zokor by referring to single-cell RNA results in mice. We discovered that spermatogenesis is arrested at the spermatocyte during the non-breeding season, which was corroborated via immunofluorescence staining results. The analysis of gene expression during different stages of meiotic prophase I has revealed that germ cell development may be arrested, starting from zygonema, during the non-breeding season. Meanwhile, we discovered that the apoptosis genes were up-regulated, leading to apoptosis in spermatocytes. To confirm that the germ cell differentiation was blocked during the non-breeding season due to a decrease in the androgen level, we used androgen receptor antagonist (flutamide) to intervene in the breeding season and found that the inner diameter of the seminiferous tubules was significantly reduced, spermatogenesis was arrested, and spermatocytes underwent apoptosis. This study revealed that spermatocytes are the terminal of germ cell differentiation in plateau zokor during the non-breeding season and that the arrest of differentiation is attributed to a decline in androgen levels. Our results complement the theoretical basis of seasonal reproduction in plateau zokor.

  • ORIGINAL ARTICLE
    Shengjing SONG , Heye CHEN , Yu ZHANG , Xiaojia ZHU , David M. IRWIN , Kai HE , Yang LIU

    Myoglobin (Mb) mediates oxygen diffusion and storage in muscle tissue and thus is important for the energy utilization and activity of animals. Birds generally have a high body temperature, and most species also possess the capability of powered flight. Both of these require high levels of aerobic metabolism. Within endothermic mammals, bats also independently evolved flight. Although the functional evolution of myoglobins in deep-diving amniote vertebrates has been well-studied, the functional evolution of myoglobin since the origins of both birds and bats is unclear. Here, with Mb-coding sequences from >200 extant amniote species, we reconstructed ancestral sequences to estimate the functional properties of myoglobin through amniote evolution. A dramatic change in net surface charge on myoglobin occurred during the origin of Aves, which might have been driven by positively selected amino acid substitutions that occurred on the lineage leading to all birds. However, in bats, no change in net surface charge occurred and instead, the Mb genes show evidence of strong purifying selection. The increased net surface charge on bird myoglobins implies an adaptation to flight-related endothermic and higher body temperatures, possibly by reducing harmful protein aggregations. Different from the findings of net surface charge, myoglobins of extant birds show lower stability compared with other amniotes, which probably accelerates the rate of oxygen utilization in muscles. In bats and other mammals, higher stability of Mb may be an alternative pathway for adaptation to endothermy, indicating divergent evolution of myoglobin in birds and bats.

  • ORIGINAL ARTICLE
    Anna ZIMIN , Sean V. ZIMIN , L. Lee GRISMER , Aaron M. BAUER , David G. CHAPPLE , Jacob DEMBITZER , Uri ROLL , Shai MEIRI

    Different substrates pose varied biomechanical challenges that select specific morphologies, such as long limbs for faster running and short limbs for balanced posture while climbing narrow substrates. We tested how gecko locomotion is affected by the microhabitat they occupy and by a key adaptation—adhesive toepads—through analyzing how those are related to limb morphology. We collected microhabitat and toepads data for over 90% of limbed gecko species, and limb measurements for 403 species from 83 of the 121 limbed gecko genera, which we then used in phylogenetic comparative analyses. Our data highlight the association of adhesive toepads with arboreality, but a phylogenetic analysis shows that this relationship is not significant, suggesting that these traits are phylogenetically constrained. Comparative analyses reveal that pad-bearing species possess shorter hindlimbs and feet, more even limb lengths, and lower crus: thigh ratios, than padless geckos, across microhabitats. Saxicolous geckos have the longest limbs and limb segments. This is probably influenced by selection for long strides, increased takeoff velocity, and static stability on inclined surfaces. Terrestrial geckos have more even hind- and forelimbs than arboreal geckos, unlike patterns found in other lizards. Our findings underline the difficulty to infer on microhabitat–morphology relationships from one taxon to another, given their differing ecologies and evolutionary pathways. We emphasize the importance of key innovation traits, such as adhesive toepads, in shaping limb morphology in geckos and, accordingly, their locomotion within their immediate environment.

  • ORIGINAL ARTICLE
    Yanting QIAO , Ning LI , Ying SONG , Xiaohui LIU , Dawei WANG

    Photoperiod, the length of daylight, has a significant impact on the physiological characteristics of seasonal breeding animals, including their somatic and gonadal development. In rodents, expression of deiodinase type II (Dio2) and III (Dio3) in the hypothalamus is crucial for responding to photoperiodic signals. However, research on the photoperiodism of hypothalamic gene expression and the corresponding regulatory mechanism in Brandt's voles living in the Mongolian steppes is limited. In this study, we gradually changed day length patterns to simulate spring (increasing long photoperiod, ILP) and autumn (decreasing short photoperiod, DSP). We compared the somatic and gonadal development of voles born under ILP and DSP and the expression patterns of five reproduction-related genes in the hypothalamus of young voles. The results showed that DSP significantly inhibited somatic and gonadal development in both female and male offspring. Compared with ILP, Dio3 expression was significantly upregulated in the hypothalamus under DSP conditions and remained elevated until postnatal week 8 in both males and females. However, there was no significant difference in the methylation levels of the proximal promoter region of Dio3 between ILP and DSP, suggesting that methylation in the proximal promoter region may not be involved in regulating the expression of Dio3. These findings suggest that hypothalamic expression of Dio3 plays a key role in the photoperiodic regulation of gonadal activity in Brandt's voles. However, it appears that CpGs methylation in the promoter region is not the main mechanism regulating Dio3 expression.

  • LETTER TO THE EDITOR
    Roberta MARTINO , Clément ZANOLLI , Darío FIDALGO , Luca PANDOLFI
  • LETTER TO THE EDITOR
    Yuhan YUAN , Xiaohan YANG , Xinyue YANGLI , Yingjian TIAN , Ying JIANG , Long JIN
  • LETTER TO THE EDITOR
    Siqiong LIU , Kexin LI , Yuxin ZHENG , Jiayang XUE , Sheng WANG , Song LI , Peng CAO , Feng LIU , Qingyan DAI , Xiaotian FENG , Ruowei YANG , Wanjing PING , Dongdong WU , Pengfei FAN , Qiaomei FU , Zehui CHEN