2021 Vol. 42, No. 2

2021-2 Contents
2021, 42(2): 1-1.
After the publication of Wang et al. (2020), we realized that there were some inappropriate statements in the content. Hereby, we correct them and apologize for any confusion this may have caused.
Following the publication of our paper (Zhang et al., 2020), it has come to our attention that we erroneously listed two funding sources unrelated to this study in the “ACKNOWLEDGEMENTS” section. Hereby, we wish to update the “ACKNOWLEDGEMENTS” section as a correction:
Research highlight
The water-to-land transition was a major step in vertebrate evolution and eventually gave rise to the tetrapods, including amphibians, reptiles, birds, and mammals. The first land invasion of our fish ancestors is considered to have occurred during the late Devonian period ~370 million years ago (Mya) (Daeschler et al., 2006). Many fossils from important transitional species, such as Tiktaalik, Acanthostega, and Ichthyostega, have helped to identify key morphological and anatomical structures crucial to vertebrate terrestrial adaptation (Coates, 1996; Johanson & Ahlberg, 2001; Shubin et al., 2006). However, homologous analyses of these body forms and structures in more ancient species have suggested that some of the morphologies related to vertebrate land dispersal were already present in early bony fish species. For instance, the presence of shoulder girdles on the articular surface of the endoskeleton in Late Lochkovian Psarolepis indicates that stem sarcopterygians already possessed an endoskeletal fin pattern similar to that of tetrapod stylopods (Zhu & Yu, 2009). In addition, primitive lungs, which originated from the respiratory pharynx and were located on the ventral side of the alimentary tracts, can be observed in several extant basal actinopterygians (bichirs, reedfish) and all extant sarcopterygians, as well as some fossils of coelacanths and salamanders (Cupello et al., 2017; Tissier et al., 2017) (Figure 1). This evidence suggests that, instead of relying on genetic innovations evolving after the first fish left their water habitat, this transition may have been accomplished by adopting physical traits and genetic components that already existed far earlier than when the transition occurred. Whether such an ancestral developmental regulatory network was present or not and how far this ancestral network can be traced in history are challenging questions for paleontologists. Three recent papers published in Cell provide new insights into this hypothesis. Wang et al. (2021) sequenced the giant genome of lungfish, the closest fish species to tetrapods, and Bi et al. (2021) sequenced the genomes of multiple early divergent ray-finned fish. Comparative genomic analyses from these two studies confirmed the presence of ancestral genetic regulatory networks that likely played essential roles in the development and evolution of various biological functions related to vertebrate land invasion. Although certain ancestral features have been lost in teleosts, the most derived fish lineage to evolve after whole-genome duplication (Sato & Nishida, 2010), they have been recreated in zebrafish by modifying their genetic makeup to reactivate the ancestral genetic network (Hawkins et al., 2021).
We recently identified a cynomolgus monkey with naturally occurring Parkinson’s disease (PD), indicating that PD may not be a uniquely human disease (Li et al, 2020). In our previous study, four lines of evidence, including typical PD clinical symptoms, pharmacological responses, pathological hallmarks, and genetic mutations, strongly supported the identification of a monkey with spontaneous PD (Figure 1). To the best of our knowledge, this is the first reported case of naturally developed PD in animals. This suggests that PD is not a disease restricted to humans, with its existence in a non-human primate providing a novel evolutionary angle for understanding PD. As a close relative to humans (Buffalo et al, 2019; Phillips et al, 2014; Yan et al, 2011), this rare case of PD in another primate species provides solid evidence that monkeys are ideal candidates for the development of a genuine “animal version of PD”, with conserved etiology and pathogenesis (Li et al, 2020). Furthermore, it allows us to compare similarities and differences in PD development between species and to understand PD pathogenesis from an evolutionary point of view.
Secretory pore-forming proteins (PFPs) have been identified in organisms from all kingdoms of life. Our studies with the toad species Bombina maxima found an interaction network among aerolysin family PFPs (af-PFPs) and trefoil factors (TFFs). As a toad af-PFP, BmALP1 can be reversibly regulated between active and inactive forms, with its paralog BmALP3 acting as a negative regulator. BmALP1 interacts with BmTFF3 to form a cellular active complex called βγ-CAT. This PFP complex is characterized by acting on endocytic pathways and forming pores on endolysosomes, including stimulating cell macropinocytosis. In addition, cell exocytosis can be induced and/or modulated in the presence of βγ-CAT. Depending on cell contexts and surroundings, these effects can facilitate the toad in material uptake and vesicular transport, while maintaining mucosal barrier function as well as immune defense. Based on experimental evidence, we hereby propose a secretory endolysosome channel (SELC) pathway conducted by a secreted PFP in cell endocytic and exocytic systems, with βγ-CAT being the first example of a SELC protein. With essential roles in cell interactions and environmental adaptations, the proposed SELC protein pathway should be conserved in other living organisms.
Epithelial ovarian cancer (EOC) is the leading cause of gynecological cancer-related mortality in the developed world. EOC is a heterogeneous disease represented by several histological and molecular subtypes. Therefore, exploration of relevant preclinical animal models that consider the heterogenic nature of EOC is of great importance for the development of novel therapeutic strategies that can be translated clinically to combat this devastating disease. In this review, we discuss recent progress in the development of preclinical mouse models for EOC study as well as their advantages and limitations.
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and coronavirus disease 2019 (COVID-19) continue to impact countries worldwide. At present, inadequate diagnosis and unreliable evaluation systems hinder the implementation and development of effective prevention and treatment strategies. Here, we conducted a horizontal and longitudinal study comparing the detection rates of SARS-CoV-2 nucleic acid in different types of samples collected from COVID-19 patients and SARS-CoV-2-infected monkeys. We also detected anti-SARS-CoV-2 antibodies in the above clinical and animal model samples to identify a reliable approach for the accurate diagnosis of SARS-CoV-2 infection. Results showed that, regardless of clinical symptoms, the highest detection levels of viral nucleic acid were found in sputum and tracheal brush samples, resulting in a high and stable diagnosis rate. Anti-SARS-CoV-2 immunoglobulin M (IgM) and G (IgG) antibodies were not detected in 6.90% of COVID-19 patients. Furthermore, integration of nucleic acid detection results from the various sample types did not improve the diagnosis rate. Moreover, dynamic changes in SARS-CoV-2 viral load were more obvious in sputum and tracheal brushes than in nasal and throat swabs. Thus, SARS-CoV-2 nucleic acid detection in sputum and tracheal brushes was the least affected by infection route, disease progression, and individual differences. Therefore, SARS-CoV-2 nucleic acid detection using lower respiratory tract samples alone is reliable for COVID-19 diagnosis and study.
Coronavirus disease 2019 (COVID-19), which is caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has spread rapidly worldwide with high rates of transmission and substantial mortality. To date, however, no effective treatments or enough vaccines for COVID-19 are available. The roles of angiotensin converting enzyme 2 (ACE2) and spike protein in the treatment of COVID-19 are major areas of research. In this study, we explored the potential of ACE2 and spike protein as targets for the development of antiviral agents against SARS-CoV-2. We analyzed clinical data, genetic data, and receptor binding capability. Clinical data revealed that COVID-19 patients with comorbidities related to an abnormal renin-angiotensin system exhibited more early symptoms and poorer prognoses. However, the relationship between ACE2 expression and COVID-19 progression is still not clear. Furthermore, if ACE2 is not a good targetable protein, it would not be applicable across a wide range of populations. The spike-S1 receptor-binding domain that interacts with ACE2 showed various amino acid mutations based on sequence analysis. We identified two spike-S1 point mutations (V354F and V470A) by receptor-ligand docking and binding enzyme-linked immunosorbent assays. These variants enhanced the binding of the spike protein to ACE2 receptors and were potentially associated with increased infectivity. Importantly, the number of patients infected with the V354F and V470A mutants has increased with the development of the SARS-CoV-2 pandemic. These results suggest that ACE2 and spike-S1 are likely not ideal targets for the design of peptide drugs to treat COVID-19 in different populations.
Allactaginae is a subfamily of dipodids consisting of four- and five-toed jerboas (Allactaga, Allactodipus, Orientallactaga, Pygeretmus, Scarturus) found in open habitats of Asia and North Africa. Recent molecular phylogenies have upended our understanding of this group’s systematics across taxonomic scales. Here, I used cranial geometric morphometrics to examine variation across 219 specimens of 14 allactagine species (Allactaga major, A. severtzovi, Orientallactaga balikunica, O. bullata, O. sibirica, Pygeretmus platyurus, P. pumilio, P. shitkovi, Scarturus aralychensis, S. euphraticus, S. hotsoni, S. indicus, S. tetradactylus, S. williamsi) in light of their revised taxonomy. Results showed no significant sexual size or shape dimorphism. Species significantly differed in cranial size and shape both overall and as species pairs. Species identity had a strong effect on both cranial size and shape. Only a small part of cranial shape variation was allometric, with no evidence of unique species allometries, and most specimens fit closely to the common allometric regression vector. Allactaga was the largest, followed by Orientallactaga, Scarturus, and finally Pygeretmus. Principal component 1 (PC1) separated O. bullata+O. balikunica+S. hotsoni (with inflated bullae along with reduced zygomatic arches and rostra) from A. major+A. severtzovi+O. sibirica (with converse patterns), while PC2 differentiated Orientallactaga (with enlarged cranial bases and rostra along with reduced zygomatic arches and foramina magna) from Scarturus+Pygeretmus (with the opposite patterns). Clustering based on the unweighted pair group method with arithmetic mean (UPGMA) contained the four genera, but S. hotsoni clustered with O. bullata+O. balikunica and O. sibirica clustered with A. major+A. severtzovi, likely due to convergence and allometry, respectively.
Although widely thought to be aggressive, solitary, and potentially cannibalistic, some spider species have evolved group-living behaviors. The distinct transition provides the framework to uncover group-living evolution. Here, we conducted a comparative transcriptomic study and examined patterns of molecular evolution in two independently evolved group-living spiders and twelve solitary species. We report that positively selected genes among group-living spider lineages are significantly enriched in nutrient metabolism and autophagy pathways. We also show that nutrient-related genes of group-living spiders convergently experience amino acid substitutions and accelerated relative evolutionary rates. These results indicate adaptive convergence of nutrient metabolism that may ensure energy supply in group-living spiders. The decelerated evolutionary rate of autophagy-related genes in group-living lineages is consistent with an increased constraint on energy homeostasis as would be required in a group-living environment. Together, the results show that energy metabolic pathways play an important role in the transition to group-living in spiders.
Letters to the editor
Deforestation represents one of the greatest threats to tropical forest mammals, and the situation is greatly exacerbated by bushmeat hunting. To construct informed conservation plans, information must be gathered about responses to habitat degradation, regeneration, and hunting over a sufficiently long period to allow demographic responses. We quantified changes in the abundance of three commonly occurring ungulate species (i.e., bushbuck, Tragelaphus scriptus; red duiker, Cephalophus sp.; blue duiker, Cephalophus monticola) at eight sites in Kibale National Park, Uganda (old growth=3; logged=3; regenerating=2) for 23 years. Changes in abundance (363 surveys totaling 1 450 km) were considered in regard to the park’s management strategy, regional economic indicators, and estimates of illegal hunting. Bushbuck abundance increased in old-growth and logged forests from 1996 to 2009, and then oscillated around this level or declined. Duiker abundance demonstrated a similar pattern, but abundance in the old-growth forests showed a general increase from 1996 to present day. Duiker abundance in the logged forests exhibited an early increase, but subsequent oscillation. Poaching signs per patrol have remained stable over the last decade, despite increases in the size of the surrounding population, cost of living, and cost of schooling, thus reflecting successful efforts in conservation education and enforcement. Our study highlights the positive impact of park establishment, patrol, and conservation efforts on ungulate populations and shows the adaptability of forest mammal populations to different management schemes.
Muntjac deer (Cervidae: Muntiacus) are often cited as an excellent model for the study of vertebrate evolution due to their fast rate of change in chromosome number among vertebrates. However, the phylogenetic relationships within Muntiacus generally, and the taxonomic status of Muntiacus gongshanensis specifically, remain unclear. Here, the phylogenetic relationships within Muntiacus were studied using mitochondrial genome (mitogenome) and cytochrome b (cyt b) segments. Our results recognize 12 species within Muntiacus and support the controversial species M. gongshanensis, M. putaoensis, and M. malabaricus. Furthermore, Bayesian inference (BI) and maximum-likelihood (ML) approaches revealed M. gongshanensis and M. crinifrons to be closely related species, with M. feae as their sister species, and M. putaoensis and M. truongsonensis to be closely related, with M. rooseveltorum as their sister species. The distribution range of M. gongshanensis was also confirmed in southwest China (Namdapha, Modong, Zayu and Gongshan) and northern Myanmar (Putao). The results of this study provide insight into the evolution of Muntiacus and further provide a molecular basis for the taxonomic evaluation of the genus in the future and fundamental data for the conservation of M. gongshanensis.
Recent studies have examined the cost of raising parasitic cuckoos and highlighted the importance of “no extra cost” in explaining the low levels of defense in hosts. To clarify the reasons for parasitization in typical hosts, we present a simple model to explore the immediate and future costs of parasitism in shaping the evolution of defense behavior in hosts. Our results suggest that any cost of parasitization is maladaptive to the host and learned egg recognition is always favored to overcome these costs. Furthermore, although facing a potential cost of mis-imprinting, learned nestling recognition may still evolve when there is a non-zero immediate cost from raising a parasitic nestling. Therefore, we contend that “no extra cost” does not provide sufficient evidence to explain the low levels of defense behavior in hosts per se.
Parents may adjust their breeding time to optimize reproductive output and reduce reproductive costs associated with unpredictable climatic conditions, especially in the context of global warming. The breeding performance of tropical bird species in response to local climate change is relatively understudied compared with that of temperate bird species. Here, based on data from 361 white-rumped munia (Lonchura striata) nests, we determined that breeding season onset, which varied from 15 February to 22 June, was delayed by drought and high temperatures. Clutch size (4.52±0.75) and daily survival rate but not egg mass (0.95±0.10 g) were negatively affected by frequent rainfall. Daily nest survival during the rainy breeding season in 2018 (0.95±0.04) was lower than that in 2017 (0.98±0.01) and 2019 (0.97±0.00). The overall nesting cycle was 40.37±2.69 days, including an incubation period of 13.10±1.18 days and nestling period of 23.22±2.40 days. The nestling period in 2018 (25.11±1.97 days) was longer than that in 2017 (22.90±2.22 days) and 2019 (22.00±2.48 days), possibly due to the cooler temperatures. Climate also affected the total number of successful fledglings, which was highest under moderate rainfall in 2017 (115 fledglings) and lowest during prolonged drought in 2019 (51 fledglings). Together, our results suggest that drought and frequent rainfall during the breeding season can decrease reproductive success. Thus, this study provides important insights into bird ecology and conservation in the context of global climate change.
We describe a new species of the genus Kurixalus, Kurixalus raoi sp. nov ., from Guizhou Province, China, based on morphological and molecular evidence. Phylogenetically, the new species is sister to K. idiootocus, but is distinguishable from all known congeners by a combination of the following characters: small body size (snout-vent length 28.2‒32.2 mm in males; 38.6 mm in female); snout rounded, with no prominence on tip; single internal vocal sac; dorsal surface brown, rough, scattered with several small warts; chin clouded with blackish marking; pair of large symmetrical dark blotches on chest; vomerine teeth present; iris brown; tibiotarsal articulation reaching center of eye; nuptial pad slight; flank rough; mandibular symphysis weak; throat skin granular; and toes moderately webbed, formula I2‒2II1.5‒3III2‒3IV3‒2V. The genetic distances between the new species and K. idiootocus were 2.9% and 5.4% for 16S rRNA and COI, respectively.
We report on a new amphibian species of the genus Micryletta from Hainan Island, China, based on morphological and molecular analyses. The new species, Micryletta immaculata sp. nov. , is diagnosed by a combination of the following morphological characters: medium-sized within genus (SVL 23.3–24.8 mm in males, n=3; 27.7–30.1 mm in females, n=2); dorsum bronze brown to reddish brown in life; dark brown spots and stripes on dorsum and flank absent; flanks largely pigmented with silver white; throat in adult males dark brown; undersides without dark patterns; outer metatarsal tubercle absent; supratympanic fold distinct; webbing between toes basal and poorly developed; tibiotarsal articulation adpressed limb reaching level of tympanum. The new species is divergent from all other congeners based on 16S rRNA gene sequences (3.0%–7.7%). Data on the natural history and male advertisement calls of the new species are provided. Following the IUCN Red List Categories and Criteria, we propose the new species to be listed as Vulnerable B1ab (iii).
A new loach species (Cypriniformes: Nemacheilidae: Yunnanilini), Yunnanilus chuanheensis sp. nov. , was caught from Chuanhe in the upper reaches of the Lixianjiang River, a tributary of the Red River in Nanjian County, Yunnan Province, China. This species is a member of the traditional Y. pleurotaenia species group based on the presence of a lateral line and cephalic lateral-line canals. It can be distinguished from other species in the Y. pleurotaenia species group by the following characters: lips without papillae, anterior and posterior nostrils separated, whole body scaled, eye diameter smaller than interorbital width, outer gill raker absent on first gill arch, eye diameter greater than 18% of head length, 10–11 inner gill rakers on first gill arch, and lateral line not extending to vertical through dorsal fin insertion. To the best of our knowledge, this is the first Yunnanilus species recorded from the Red River drainage.
Somatic mutations are a large category of genetic variations, which play an essential role in tumorigenesis. Detection of somatic single nucleotide variants (SNVs) could facilitate downstream analysis of tumorigenesis. Many computational methods have been developed to detect SNVs, but most require normal matched samples to differentiate somatic SNVs from the normal state, which can be difficult to obtain. Therefore, developing new approaches for detecting somatic SNVs without matched samples are crucial. In this work, we detected somatic mutations from individual tumor samples based on a novel machine learning approach, svmSomatic, using next-generation sequencing (NGS) data. In addition, as somatic SNV detection can be impacted by multiple mutations, with germline mutations and co-occurrence of copy number variations (CNVs) common in organisms, we used the novel approach to distinguish somatic and germline mutations based on the NGS data from individual tumor samples. In summary, svmSomatic: (1) considers the influence of CNV co-occurrence in detecting somatic mutations; and (2) trains a support vector machine algorithm to distinguish between somatic and germline mutations, without requiring normal matched samples. We further tested and compared svmSomatic with other common methods. Results showed that svmSomatic performance, as measured by F1-score, was significantly better than that of others using both simulation and real NGS data.