Morphological Adaptation of Cave-Dwelling Ground Beetles in China Revealed by Geometric Morphometry (Coleoptera, Carabidae, Trechini)
by
,
Mengzhen Chen
1,†, 
Wanru Guo
1,†,
Sunbin Huang
1,2,
Xiaozhu Luo
1,3,
Mingyi Tian
1,* and
Weixin Liu
1,* 1
Department of Entomology, College of Plant Protection, South China Agricultural University, 483 Wushan Road, Guangzhou 510642, China
2
Mécanismes Adaptatifs et Évolution (MECADEV), Muséum National d’Histoire Naturelle, CP50, 57 Rue Cuvier, 75005 Paris, France
3
Institute of Zoology and Evolutionary Research, Friedrich Schiller University Jena, Erbertstr. 1, 07743 Jena, Germany
*
Authors to whom correspondence should be addressed.
†
These authors have contributed equally to this work.
Insects 2021, 12(11), 1002; https://doi.org/10.3390/insects12111002
Submission received: 28 September 2021
/
Revised: 29 October 2021
/
Accepted: 30 October 2021
/
Published: 8 November 2021
(This article belongs to the Section Insect Systematics, Phylogeny and Evolution)
Abstract
:Simple Summary
Cavernicolous ground beetles dwelling in China are one of the most diverse and underground-adapted coleopteran group in the world. The tribe Trechini is, among them, the most representative group constituting over 170 known species with a narrow and elongated body and long appendages or a stout body and short appendages. However, very little information about their morphology has been explored. The aim of this study was to analyze the morphological adaptations of this group using geometric morphological methods. The beetles were divided into four different morphological types, including aphaenopsian, semi-aphaenopsian, anophthalmic, and surface-dwelling, and the analysis is based on the morphology of their head, pronotum, and elytra. Our findings indicate that the overall morphological variation of cave trechine beetles has gradually specialized from an anophthalmic to semi-aphaenopsian to aphaenopsian type. Different types have different directions of variation in the head, pronotum, and elytra, but the pronotum is more differentiated and morphologically diverse than the head and elytra.
Abstract
Cave-dwelling ground beetles in China represent the most impressive specific diversity and morphological adaptations of the cavernicolous ground beetles in the world, but they have not been systematically examined in quantitative terms. The present study focuses on the application of geometric morphological methods to address the morphological adaptations of the tribe Trechini, the most representative group in China. We have employed a geometric morphometry analysis of the head, pronotum, and elytra of 53 genera of Trechini, including 132 hypogean and 8 epigean species. Our results showed that the overall morphological variation of cave carabids has gradually specialized from an anophthalmic to semi-aphaenopsian to aphaenopsian type. There were extremely significant differences (p < 0.01) among four different adaptive types including aphaenopsian, semi-aphaenopsian, anophthalmic, and surface-dwelling Trechini when their adaptability to a cave environment was used as the basis for grouping. Furthermore, there were differences in the phenotypic tree of the head, pronotum, and elytra, and an integrated morphology. To the best of our knowledge, this is the first report on the analysis of the head, pronotum, and elytra of four different adaptive types of ground beetles in order to clarify the morphological adaptations of cavernicolous carabids to the cave environment.
1. Introduction
China is very rich in cave-dwelling ground beetles. At present, 202 species of cave carabids belonging to 8 tribes and 71 genera have been recorded, among which the Trechini is the most diverse group including 175 species from 63 genera [1,2]. All of them are troglobionts and completely lack eyes, except for four troglophiles with more or less degenerated eyes [3]. In addition to the disappearance of their eyes, cavernicolous carabids underwent morphological modifications during long-term adaptation to the subterranean environment. These are manifested in the loss of pigment and metathoracic wings, as well as their more slender body and thin legs [4,5]. According to the adaptability of characteristic appearances and biological information, cave trechine beetles were divided into three morphological types [6,7,8]: aphaenopsian, semi-aphaenopisan, and anophthalmic (Figure 1). The former means that these carabids have an extreme elongation of their body and appendages, while the latter refers to their stout body and shorter appendages. The semi-aphaenopsian is considered to be a transitional type, with morphological characteristics lying between the above two. The surface-dwelling trechine beetles have darker body color and compound eyes (Figure 1).
Geometric morphometry is an approach that relies on the quantitative analysis of the geometry of the target structure and the further performance of statistical analyses [9]. Different types of data, such as landmark coordinates, outline curves, and surfaces are used to define the shape [10]. The original morphological information is usually obtained through Cartesian coordinates, which are used to remove the interference of non-morphological variation in the analysis so that the punctuation overprint analysis of all samples can be visualized and displayed [11]. Geometric morphometry began to be used in the 1980s, and in the 21st century it has been widely used in entomology, medicine, archaeology, and other fields [12,13,14]. Recently, geometric morphometry has developed from two-dimensional to three-dimensional. Three-dimensional scanning, electron microscope scanning, micro-CT scanning, etc., provide advanced technical support for the development of geometric morphometry [15,16,17].
The application of geometric morphometry to coleopteran insects is very extensive. It is often used to explore morphological differences between species with sexual dimorphism [18,19], intersubspecies, sister groups [20,21], and high-level categories [22,23]. It is also possible to infer the ancestral form of an existing taxa in order to study its origin and evolution [24]. Geometric morphometry has gradually been applied to different groups of Coleoptera, including Carabidae [25,26,27], Lucanidae, Chrysomelidae [28], Scarabaeidae [29,30,31], and Silphidae [32]. However, studies of the geometric morphometry of cave-dwelling ground beetles have rarely been reported [33].
Based on a geometric morphometric approach, the present paper provides, for the first time, an analysis of the head, pronotum, and elytra of four different adaptive types of ground beetles in order to clarify the morphological adaptations of cavernicolous carabids to the cave environment. In addition, the phenotypic relationship was obtained with a clustering analysis in the genetic category to explore the morphological evolution of cave-dwelling ground beetles.
2. Materials and Methods
2.1. Studied Materials
For the materials used in this study, we implemented the following principles: (1) Sampling as many genera and species as possible, including type species. (2) We did not deal with subgenus separately; species taxonomic treatment was based on the latest publications. (3) We used bibliographic data to obtain the morphological adaptation types of known taxa, e.g., [34,35,36,37,38].
2.2. Geometric Morphometric Approach
2.2.1. Image Acquisition
Photographs of existing samples were taken with a Keyence VHX-5000 digital microscope (Figure S1). Due to the lack of specimens for 44 species, images were obtained from related original literature, e.g., [42,43,44] (Figure S1). For Minimaphaenops (Enshiaphaenops) senecali Deuve, 2016, we gathered the data from the specimen we collected as well as the additional figure of the type specimen from the original publication. After editing using Adobe Photoshop CS6, we imported the data into tps-Util 1.78 [45].
2.2.2. Landmark Data
The shape of the head, pronotum, and elytra and the positions of stable pores on the elytra were chosen as morphological indicators. We selected the configurations of 50 semilandmarks of each object, except for the stable pores on the elytra, which were represented by 6 landmarks (Figure 2). The landmarks and semilandmarks in each image were digitized using the tps-Dig 2.31 software (Landmark Data S1). The Tps-Small 1.34 software [46] was used to detect the data correlation of the.tps files after the landmarks to verify whether the data correlation met the requirements.
2.2.3. Statistical Analysis
The morphological data obtained by the standardized processing of different cave environment-adapted types were imported into the MorphoJ 1.07A software. Generalized Procrustes Analysis (GPA) was used to perform Procrustes superimposition on the overall samples to extract shape variables [47,48]. We used calculational processing to ensure that the sum of the squares of the distances between landmarks of the same serial number was minimized. Additionally, we calculated the overall average shape to compare the degree of difference between the individual and overall average shape (measured by Procrustes distance). On this basis, we applied principal component analysis (PCA).
We selected the first two principal components (PC) to construct scatterplots to show the morphological differences of carabids in different cave environment adaptation types. An energy map of the extreme points of the coordinate origin arrangement was obtained from a thin-plate spline (TPS) analysis using the MorphoJ 1.07A software, where differences in the landmarks were displayed in a visual form.
On the basis of PCA, we set the different cave environment adaptation types as the basis for grouping and performed canonical variate analysis (CVA). The results were displayed through the Mahalanobis distance and Procrustes distance.
2.2.4. Clustering Analysis
The original TPS file was split into 53 subfiles according to genera using the tps-Util 1.78 software; then we used the tps-Super 2.05 software to calculate the average form of each genus. Procrustes distances between genera were preformed using the tps-Small 1.34 software; then we used the unweighted group averaging method (UPGMA) in the NTSYSpc 2.10e software [49] to analyze the Procrustes distance matrix.
3. Results
3.1. Internal Correlation of the Original Data
The original data were converted from camber Kendall space to Euclidean tangent space. For the head, pronotum, and elytra, the correlation coefficients of the data before and after the conversion were 0.999995, 0.999992, and 1.000000, respectively, which met the requirements.
3.2. PCA of the Morphological Variation in Head, Pronotum and Elytra
Principal component analysis was performed on the morphological data of the head, pronotum, and elytra for 141 species of carabid beetles, with 96, 96, and 108 principal components being obtained, respectively. Among them, the first principal component (PC1) accounted for 89.86%, 84.95%, and 39.35% of the overall variance, while the second principal component (PC2) accounted for 3.94%, 7.75%, and 27.20%, respectively. Using PC1 and PC2, which affect the morphological variation, as the abscissa and ordinate, respectively, a scatterplot of the morphological variation was obtained, and a 90% equal frequency ellipse was constructed based on the cave adaptation type of these carabid beetles (Figure 3a,c,e).
From the perspective of the morphological variation of the head (Figure 3a) and pronotum (Figure 3c), it was found that the aphaenopsian had no overlap and could be distinguished well from anophthalmic and surface-dwelling carabid beetles. The semi-aphaenopsian carabid beetle type was between the aphaenopsian and anophthalmic types and was more similar to the anophthalmic type because of its larger overlaps. The latter was closer to the surface-dwelling carabid beetles. Regarding the morphological variation of the elytra (Figure 3e), these four types overlapped more overall. No significant differences were found between elytra of the semi-aphaenopsian, aphaenopsian, and anophthalmic types.
The energy map of the coordinate origin and the extreme points of the PCA scatterplot of carabid beetles’ head, pronotum, and elytra (Figure 3b,d,f) show that the length/width ratio of the head and pronotum has a tendency to decrease significantly, while their lateral edges expand outward in the positive direction of PC1. The widest point of the head moves to the front, but the front edge of the pronotum tends to be wider than the rear edge. Elytra tend to be more slender and the scutellum appears to be narrower. The anterior of the edge side of the elytra has a tendency to undergo adduction, with the shoulders disappearing and the position of the hair pores moving to the distal end of the elytra. In the positive direction of PC2, the posterior edge of the head is sunken inward and the front and caudal corners of the pronotum tend to become acute from an obtuse angle. The first four elytra hair pores are more scattered and the last three are closer together.
3.3. CVA of the Morphological Variation in Head, Pronotum, and Elytra
According to the results of the PCA, CVA was used to analyze the morphological variation in the distances of the head, pronotum, and elytra among all the genera of carabid beetles. The results showed that the Mahalanobis distance and Procrustes distance between aphaenopsian and surface-dwelling types were largest when adaptability to a cave environment was used as the basis for grouping. For the head, pronotum, and elytra, the maximum Mahalanobis distance (Table 1) was 28.5719, 20.8313, and 20.7926, respectively, while the maximum Procrustes distance (Table 2) was 0.3429, 0.3258, and 0.1032, respectively.
The Mahalanobis distance (Table 3) and Procrustes distance (Table 3) of the head, pronotum, and elytra were tested to determine the significance of the differences. It was shown that the four different types (aphaenopsian, semi-aphaenopsian, anophthalmic, and surface-dwelling carabid beetles) had high significant differences from each other (p < 0.01).
3.4. The Phenotypic Evolutionary Relationship between Cave Trechini Genera
Based on the Procrustes distance matrix of the average morphology among 53 genera of carabid beetles, a cluster analysis was performed to construct a morphological phenotypic tree, including the head, pronotum, elytra, and all three (Figure 4). The results revealed that there were differences between the four phenotypic trees, but the variation trend of the head and the integrated morphological phenotypic tree was relatively close. When the 53 genera branched for the first time, the aphaenopsian and semi-aphaenopsian genera clustered into a clade, while the anophthalmic and surface-dwelling genera of carabid beetles clustered into another clade.
In the head phenotypic tree (Figure 4a), Sidublemus was the first to be differentiated into a single branch. Dongodytes, Sinaphaenops, Giraffaphaenops, and Pilosaphaenops were all found to be closely related. However, Shuangheaphaenops, Uenotrechus, Xuedytes, Yanzaphaenops, and Minimaphaenops were mixed together with mostly semi-aphaenopsian genera carabid beetles. From the integrated phenotypic tree (Figure 4d), it could be seen that Giraffaphaenops and Xuedytes were the earliest to differentiate, and they were located far from other genera. The relationship between Yanzaphaenops of the aphaenopsian and semi-aphaenopsian group was relatively close, while Wanhuaphaenops of the anophthalmic group had a close relationship to those of the aphaenopsian group.
In the pronotum phenotypic tree (Figure 4b), all the aphaenopsian group except for Yanzaphaenops was combined into a clade with Wanhuaphaenops, Shenaphaenops, and Huoyanodytes. The remaining three types of carabids genera were clustered together, while about 1/3 of the anophthalmic type were grouped with surface-dwelling carabid beetles in another clade. The result of the elytra phenotypic tree (Figure 4c) showed that Dianotrechus was the first to be differentiated into a single branch. The aphaenopsian group and a small part of the semi-aphaenopsian group were clustered into a clade. Among them, Dongodytes is closely related to Xuedytes, but the same highly specialized Sinaphaenops was far away from the other genera in the aphaenopsian group. Part of the semi-aphaenopsian and anophthalmic groups were grouped together with surface-dwelling carabids.
4. Discussion
4.1. Morphological Variation Direction of Cave-Adapted Trechine Beetles
The highly specialized morphological characteristics of cave-dwelling ground beetles have long attracted the attention of researchers [50]. Most previous studies in this area have focused on changes in the morphology of cave-dwelling ground beetles after their long-term adaptation to cave life [51,52,53]. The present research is the first to attempt to study the morphological adaptation and variation direction of cave-dwelling ground beetles using geometric morphological analysis.
In the extreme environment of caves, animals often show the adaptive characteristics of convergent evolution due to environmental pressure [54,55]. Luo et al. [56,57] found that the cave-dwelling S. wangorum shows a distinct head posterior constriction and elongated pronotum combined with long and slender legs. Our results showed that the more slender their body is the higher the degree to which the ground beetles had adapted to the cave environment. This is mainly manifested in the fact that the widest point of the head gradually moves to the front, while the anterior edge of the pronotum tends to be narrower than the posterior edge in surface-dwelling compared to aphaenopsian carabids. Surprisingly, there is little available information concerning the elytra vitiation of cavernicolous carabids or other beetles [58]. We found that the position of the hair pores gradually moved towards the edge of the elytra, except for the scutellum, with the elytra becoming slenderer in cave carabids. One of the reasons why elytra is slenderer is a consequence of reducing or the disappearance of hind wings (also known as humeral calli) [59], and this situation is more distinct among the cave-dwelling species, especially the highly specialized ones.
In addition, aphaenopsian species mostly wander on stalactite walls or roofs in complete darkness [60], while semi-aphaenopsian species run on low rock walls or along the ground [61]. Anophthalmic species often live under small rocks or under damp dead wood in caves, and their habits are relatively close to those of surface-dwelling species [62,63,64]. It is speculated that the extension of the head and pronotum of cave-adapted ground beetles effectively increases the flexibility of the head, which may help this species to find prey in caves where food is scarce [65]. In contrast, surface-dwelling carabids may face great survival challenges [66,67] and their strong bodies will help them to fight and escape when faced with threats.
4.2. Geometric Morphology Analysis to Judge the Phylogeny of Cavernicolous Carabids
The molecular phylogeny of cave Trechini in China was analyzed based on two mitochondrial and two nuclear genes [68]. The preliminary study showed that the Chinese cave Trechini of Carabidae does not form a monophyletic lineage but rather is composed of four main independent evolutionary clades, each of which contains at least one highly convergent troglomorphic species.
In our study, certain differences exist in the morphological phenotypic trees of the head, pronotum, and elytra based on the Procrustes distance of carabids. For example, typical aphaenopsian genera—such as Dongodytes, Giraffaphaenops, Sinaphaenops, and Xuedytes—show extreme morphological specialization, but they are not clustered into same clade phylogenetically (Figure 4) [69]. Moreover, the semi-aphaenopsian genera of Shenaphaenops and Huoyanodytes and the anophthalmic type of Wanhuaphaenops are more closely related to the aphaenopsian type. A similar situation was also found in the Pyrenean subterranean Trechini, where the phylogenetic relationship between species of the same morphological type was not found to be close [70]. It may therefore be inferred that various Trechini lineages were settled multiple times independently in caves and underwent parallel morphological changes.
Furthermore, we did not classify the subgenus as an independent taxon in the present study, but the morphological differences between some subgenera in the same genus are relatively considerable. These differences may have a certain impact on the results of overall average shape.
Moreover, the length between the clade of Giraffaphaenops + Xuedytes and other genera is extensive in the integrated morphological phenotypic tree (Figure 4). This may have been caused by long periods of geographical isolation, or there may still be large gaps between these two genera and others. Future geometric morphometry of research for these groups could focus on adding the missing new genera and combining molecular phylogeny and biogeography for analysis.
Supplementary Materials
The following are available online at https://www.mdpi.com/article/10.3390/insects12111002/s1, Figure S1: Photographs of samples, Landmark Data S1: Semi-landmarks of samples.
Author Contributions
Conceptualization, M.T., S.H., X.L. and W.L; methodology, M.C.; software, M.C.; validation, W.G. and W.L.; formal analysis, M.C., W.G. and W.L.; investigation, M.T., S.H., M.C. and W.L.; resources, M.T., S.H., M.C. and W.L.; data curation, M.T., S.H., M.C., W.G. and W.L.; writing—original draft preparation, M.C., W.G. and W.L; writing—review and editing, M.T., S.H., M.C., W.L., W.G. and X.L.; visualization, W.L. and W.G.; supervision, M.T. and W.L.; project administration, M.T. and W.L.; funding acquisition, M.T. and W.L. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by the National Natural Science Foundation of China, grant number 41871039.
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
Not applicable.
Acknowledgments
We greatly appreciated Huang Zhengzhong (Institute pf Zoology, Chinese Academy of Science) and Ge Zhentai (South China Agricultural University), who provided help with using the geometric morphology analysis software. We would like to thank the caving team members of SCAU for their assistance with fieldwork.
Conflicts of Interest
The authors declare no conflict of interest.
Appendix A
Table A1.
Basal information of the studied specimens used in the geometric morphometric analysis.
| No. | Species | Locality | Adaptive Type |
|---|---|---|---|
| 1 | Dongodytes (Dongodytes) baxian Tian, 2011 | Guangxi, Du’an County | aphaenopsian |
| 2 | D. (D.) elongatus Tian, Yin & Huang, 2014 | Guangxi, Du’an County | aphaenopsian |
| 3 | D. (D.) fowleri Deuve, 1993 | Guangxi, Bama County | aphaenopsian |
| 4 | D. (D.) giraffa Uéno, 2005 | Guangxi, Tian’e County | aphaenopsian |
| 5 | D. (D.) grandis Uéno, 1998 | Guangxi, Fengshan County | aphaenopsian |
| 6 | D. (D.) lani Tian, Yin & Huang, 2014 | Guangxi, Du’an County | aphaenopsian |
| 7 | D. (D.) tonywhitteni Yang, Huang & Tian, 2018 | Guangxi, Bama County | aphaenopsian |
| 8 | D. (D.) troglodytes Tian, Yin & Huang, 2014 | Guangxi, Du’an County | aphaenopsian |
| 9 | D. (Dongodytodes) brevipenis Tian, Yin & Huang, 2014 | Guangxi, Du’an County | aphaenopsian |
| 10 | D. (D.) deharvengi Tian, 2011 | Guangxi, Du’an County | aphaenopsian |
| 11 | D. (D.) inexpectatus Tian, Yin & Huang, 2014 | Guangxi, Du’an County | aphaenopsian |
| 12 | D. (D.) jinzhuensis Tian, Yin & Huang, 2014 | Guangxi, Du’an County | aphaenopsian |
| 13 | D. (D.) yaophilus Tian, Yin & Huang, 2014 | Guangxi, Dahu County | aphaenopsian |
| 14 | Giraffaphaenops clarkei Deuve, 2002 | Guangxi, Leye County | aphaenopsian |
| 15 | G. yangi Tian & Luo, 2015 | Guangxi, Tianlin County | aphaenopsian |
| 16 | M. (Enshiaphaenops) senecali Deuve, 2016 | Hubei, Enshi Autonomous Prefecture | aphaenopsian |
| 17 | M. (Minimaphaenops) lipsae Deuve, 1999 | Chongqing, Fengjie County | aphaenopsian |
| 18 | Pilosaphaenops pilosulus Deuve & Tian, 2008 | Guangxi, Huanjiang County | aphaenopsian |
| 19 | P. whitteni Tian, 2010 | Guangxi, Huanjiang County | aphaenopsian |
| 20 | Shuangheaphaenops elegans Tian, 2017 | Guizhou, Suiyang County | aphaenopsian |
| 21 | Sinaphaenops (Dongaphaenops) xuxiakei Deuve & Tian, 2014 | Guizhou, Pan County | aphaenopsian |
| 22 | S. (Sinaphaenops) banshanicus Tian, Chen & Tang, 2017 | Guizhou, Guiding County | aphaenopsian |
| 23 | S. (S.) gracilior Uéno & Ran, 1998 | Guizhou, Libo County | aphaenopsian |
| 24 | S. (S.) lipoi Chen, Huang & Tian, 2020 | Guizhou, Guiyang City | aphaenopsian |
| 25 | S. (S.) mirabilissimus Uéno & Wang, 1991 | Guizhou, Libo County | aphaenopsian |
| 26 | S. (S.) mochongensis Tian & Huang, 2015 | Guizhou, Duyun City | aphaenopsian |
| 27 | S. (S.) orthogenys Uéno, 2002 | Guizhou, Sandu County | aphaenopsian |
| 28 | S. (S.) wangorum Uéno & Ran, 1998 | Guizhou, Libo County | aphaenopsian |
| 29 | S. (S.) yaolinensis Tian, Chen & Yang, 2017 | Guizhou, Duyun City | aphaenopsian |
| 30 | S. (Thaumastaphaenops) bidraconis Uéno, 2002 | Guizhou, Ziyun County | aphaenopsian |
| 31 | S. (T.) pulcherrimus Magrini, Vanni & Zanon, 1997 | Guizhou, Ziyun County | aphaenopsian |
| 32 | Uenotrechus deuvei Tian & Chen, 2017 | Guangxi, Du’an County | aphaenopsian |
| 33 | U. gejianbangi Tian & Wei, 2017 | Guangxi, Huanjiang County | aphaenopsian |
| 34 | U. liboensis Deuve & Tian, 1999 | Guizhou, Maolan County | aphaenopsian |
| 35 | U. nandanensis Deuve & Tian, 2010 | Guizhou, Nandan County | aphaenopsian |
| 36 | Xuedytes bellus Tian & Huang, 2017 | Guangxi, Du’an County | aphaenopsian |
| 37 | Yanzaphaenops hirundinis Uéno, 2005 | Hubei, Shennongjiia | aphaenopsian |
| 38 | Aspidaphaenops dudou Tian & Huang, 2018 | Guizhou, Xingyi County | semi-aphaenopsian |
| 39 | A. masakii Uéno, 2006 | Guizhou, Xingyi County | semi-aphaenopsian |
| 40 | A. reflexus Uéno, 2006 | Guizhou, Ceheng County | semi-aphaenopsian |
| 41 | A. volatidraconis Uéno, 2006 | Guizhou, Xingyi County | semi-aphaenopsian |
| 42 | A. xiongda Tian & Huang, 2018 | Guizhou, Anlong County | semi-aphaenopsian |
| 43 | Boreaphaenops angustus Uéno, 2002 | Hubei, Shennongjiia | semi-aphaenopsian |
| 44 | Guiaphaenops deuvei Tian, Feng & Wei, 2017 | Guangxi, Lingyun County | semi-aphaenopsian |
| 45 | G. lingyunensis Deuve, 2002 | Guangxi, Lingyun County | semi-aphaenopsian |
| 46 | Guizhaphaenops (Guizhaphaenops) giganteus Uéno, 2000 | Guangxi, Shuicheng County | semi-aphaenopsian |
| 47 | G. (G.) lipsorum Deuve, 1999 | Yunnan, Zhenxiong County | semi-aphaenopsian |
| 48 | G. (G.) pouillyi Deuve & Queinnec, 2014 | Guizhou, Pan County | semi-aphaenopsian |
| 49 | G. (G.) striatus Uéno, 2000 | Guizhou, Liupanshui City | semi-aphaenopsian |
| 50 | G. (G.) zhijinensis Uéno & Ran, 2004 | Guizhou, Zijin County | semi-aphaenopsian |
| 51 | G. (G.) zorzini Vigna Taglianti, 1997 | Guangxi, Shuicheng County | semi-aphaenopsian |
| 52 | G. (Semiaphaenops) lipsorum zunyiensis Deuve & Tian, 2018 | Yunnan, Zhenxiong County | semi-aphaenopsian |
| 53 | G. (S.) martii Deuve, 2001 | Yunnan, Zhenxiong County | semi-aphaenopsian |
| 54 | G. (S.) yudongensis Deuve & Tian, 2016 | Yunnan, Zhenxiong County | semi-aphaenopsian |
| 55 | Huoyanodytes tujiaphilus Tian & Huang, 2016 | Hunan, Longshan County | semi-aphaenopsian |
| 56 | Jiangxiaphaenops longiceps Uéno & Clarke, 2007 | Jiangxi, Shangrao City | semi-aphaenopsian |
| 57 | Luoxiaotrechus deuvei Tian & Yin, 2013 | Hunan, You County | semi-aphaenopsian |
| 58 | L. yini Tian & Huang, 2015 | Jiangxi, Pingxiang City | semi-aphaenopsian |
| 59 | Plesioaphaenops annae Deuve & Tian, 2011 | Guangxi, Longlin County | semi-aphaenopsian |
| 60 | Shenaphaenops humeralis Uéno, 1999 | Guangxi, Shuicheng County | semi-aphaenopsian |
| 61 | Shiqianaphaenops majusculus Uéno, 1999 | Guizhou, Shiqian County | semi-aphaenopsian |
| 62 | Toshiaphaenops globipennis Uéno, 1999 | Hubei, Xianfeng County | semi-aphaenopsian |
| 63 | T. ovicollis Uéno, 1999 | Hunan, Longshan County | semi-aphaenopsian |
| 64 | Zhijinaphaenops gravidulus Uéno & Ran, 2002 | Guizhou, Zijin County | semi-aphaenopsian |
| 65 | Z. haozhicus Deuve & Tian, 2018 | Guizhou, Zijin County | semi-aphaenopsian |
| 66 | Z. jingliae Deuve & Tian, 2015 | Guizhou, Xifeng County | semi-aphaenopsian |
| 67 | Z. lii Uéno & Ran, 2002 | Guizhou, Zijin County | semi-aphaenopsian |
| 68 | Z. liuae Deuve & Tian, 2015 | Guizhou, Xifeng County | semi-aphaenopsian |
| 69 | Z. multisetifer Deuve & Tian, 2018 | Guizhou, Bijie City | semi-aphaenopsian |
| 70 | Z. pubescens Uéno & Ran, 2002 | Guizhou, Zijin County | semi-aphaenopsian |
| 712 | Z. wenganicus Deuve & Tian, 2018 | Guizhou, Wengan County | semi-aphaenopsian |
| 72 | Z. zunyicus Deuve & Tian, 2018 | Guizhou, Zhunyi City | semi-aphaenopsian |
| 73 | Bathytrechus rueci Uéno, 2005 | Guangxi, Leye County | anophthalmic |
| 74 | Cathaiaphaenops (Amygdalotrechus) amplipennis Uéno, 2000 | Hubei, Xianfeng County | anophthalmic |
| 75 | C. (A.) chuandongziensis Deuve, 1999 | Hubei, Banqiao Town | anophthalmic |
| 76 | C. (A.) cychroides Deuve & Tian, 2016 | Hubei, Lichuan City | anophthalmic |
| 77 | C. (A.) draconis Deuve, 1999 | Chongqing, Fengjie County | anophthalmic |
| 78 | C. (A.) enshiensis Deuve & Tian, 2016 | Hubei, Banqiao Town | anophthalmic |
| 79 | C. (A.) lagredeae Deuve, 2016 | Hubei, Enshi Autonomous Prefecture | anophthalmic |
| 80 | C. (A.) lynchae Deuve & Tian, 2008 | Hubei, Jianshi County | anophthalmic |
| 81 | C. (A.) vignatagliantii Deuve, 1999 | Chongqing, Fengjie County | anophthalmic |
| 82 | C. (Cathaiaphaenops) delprati Deuve, 1996 | Hunan, Longshan County | anophthalmic |
| 83 | Cimmeritodes (Cimmeritodes) huangi Deuve, 1996 | Hunan, Longshan County | anophthalmic |
| 84 | C. (Dianocimmerites) crassifemoralis Deuve & Tian, 2016 | Yunnan, Zhenxiong County | anophthalmic |
| 85 | C. (Shimenrites) shimenensis Deuve & Tian, 2017 | Hunan, Shimen County | anophthalmic |
| 86 | C. (Xiangcimmerites) zhongfangensis Deuve & Tian, 2016 | Hunan, Zhongfang County | anophthalmic |
| 87 | C. (Zhecimmerites) parvus Tian & Li, 2016 | Anhui, Chaohu City | anophthalmic |
| 88 | C. (Z.) zhejiangensis Deuve & Tian, 2015 | Zhejiang, Changshan County | anophthalmic |
| 89 | Deuveaphaenops (Deuveaphaenops) qimenxicus Tian & Huang, 2017 | Chongqing, Wulong District | anophthalmic |
| 90 | D. (Furongius) gelaophilus Tian & Huang, 2017 | Guizhou, Zhunyi City | anophthalmic |
| 91 | Dianotrechus gueorguievi Tian, 2016 | Yunnan, Anning City | anophthalmic |
| 92 | Dongoblemus kemadongicus Deuve & Tian, 2016 | Yunnan, Zhenxiong County | anophthalmic |
| 93 | Graciliblemus lipingensis Deuve & Tian, 2016 | Guizhou, Liping County | anophthalmic |
| 94 | Jiulongotrechus pubescens Tian, Huang & Wang, 2015 | Guizhou, Tongren City | anophthalmic |
| 95 | Junaphaenops tumidipennis Uéno, 1997 | Yunnan, Kunming City | anophthalmic |
| 96 | Libotrechus duanensis Lin & Tian, 2014 | Guangxi, Dahu County | anophthalmic |
| 97 | L. nishikawai Uéno, 1998 | Guizhou, Libo County | anophthalmic |
| 98 | Microblemus rieae Uéno, 2007 | Zhejiang, Jinghua City | anophthalmic |
| 99 | Oodinotrechus (Oodinotrechus) kishimotoi Uéno, 1998 | Guizhou, Libo County | anophthalmic |
| 100 | O. (O.) liyoubangi Tian, 2014 | Guangxi, Huanjiang County | anophthalmic |
| 101 | O. (Pingleotrechus) yinae Sun & Tian, 2015 | Guangxi, Pingle County | anophthalmic |
| 102 | Qianaphaenops (Qianaphaenops) emersoni Tian & Clarke, 2012 | Guizhou, Yanhe County | anophthalmic |
| 103 | Q. (Q.) longicornis Uéno, 2000 | Guizhou, Fenggang County | anophthalmic |
| 104 | Q. (Q.) pilosus Uéno, 2000 | Guizhou, Jiangkou County | anophthalmic |
| 105 | Q. (Q.) rotundicollis Uéno, 2000 | Guizhou, Sinan County | anophthalmic |
| 106 | Q. (Q.) tenuis Uéno, 2000 | Guizhou, Fenggang County | anophthalmic |
| 107 | Q. (Qiandongaphaenops) variabilis Tian, Huang & Wang, 2015 | Guizhou, Cengong County | anophthalmic |
| 108 | Q. (Tiankengius) xigouicus Tian & Huang, 2018 | Shanxi, Hanzhong City | anophthalmic |
| 109 | Qianotrechus (Qianotrechus) fani Uéno, 2003 | Sichuan, Gulin County | anophthalmic |
| 110 | Q. (Q.) laevis Uéno, 2000 | Guizhou, Zhengan County | anophthalmic |
| 111 | Q. (Q.) magnicollis Uéno, 2000 | Guizhou, Suiyang County | anophthalmic |
| 112 | Q. (Q.) tenuicollis cheni Uéno, 2003 | Guizhou, Suiyang County | anophthalmic |
| 113 | Q. (Sanwangius) rowselli, Tian & Chen, 2019 | Chongqing, Wulong District | anophthalmic |
| 114 | Satotrechus longlinensis Deuve & Tian, 2011 | Guangxi, Longlin County | anophthalmic |
| 115 | S. rieae Uéno, 2006 | Guizhou, Anlong County | anophthalmic |
| 116 | Shenoblemus minusculus Tian & Fang, 2020 | Anhui, Huangshan City | anophthalmic |
| 117 | Shilinotrechus fusiformis Uéno, 2003 | Yunnan, Shilin County | anophthalmic |
| 118 | S. intricatus Huang & Tian, 2015 | Yunnan, Yiliang County | anophthalmic |
| 119 | Shuaphaenops parvicollis Uéno, 1999 | Chongqing, Jinfoshan | anophthalmic |
| 120 | Sichuanotrechus albidraconis Uéno, 2006 | Sichuan, Jiangyou City | anophthalmic |
| 121 | S. dakangensis Huang & Tian, 2015 | Sichuan, Jiangyou City | anophthalmic |
| 122 | Sidublemus solidus Tian & Yin, 2013 | Hunan, Guidong County | anophthalmic |
| 123 | Sinotroglodytes bedosae Deuve, 1996 | Hunan, Longshan County | anophthalmic |
| 124 | S. hygrophilus Uéno, 2009 | Hunan, Sangzhi County | anophthalmic |
| 125 | S. yanwangi Huang, Tian & Faille, 2020 | Hubei, Yichang City | anophthalmic |
| 126 | Superbotrechus bennetti Deuve & Tian, 2009 | Hubei, Yichang City | anophthalmic |
| 127 | Tianeotrechus trisetosus Tian & Tang, 2016 | Guangxi, Tian’e County | anophthalmic |
| 128 | Tianzhuaphaenops jinshanensis Zhao & Tian, 2016 | Guizhou, Tianzhu County | anophthalmic |
| 129 | Wanhuaphaenops zhangi Tian & Wang, 2016 | Hunan, Chenzhou City | anophthalmic |
| 130 | Wanoblemus wui Tian & Fang, 2016 | Anhui, Xuancheng City | anophthalmic |
| 131 | Wulongoblemus tsuiblemoides Uéno, 2007 | Zhejiang, Jiangshan City | anophthalmic |
| 132 | Yunotrechus diannanensis Tian & Huang, 2014 | Yunnan, Maguan County | anophthalmic |
| 133 | Agonotrechus spinangulus Belousov, Kabak & Liang, 2019 | Sichuan, Muli County | surface-dwelling |
| 134 | Protrechiama crassipes Uéno, 1997 | Sichuan, Meigu County | surface-dwelling |
| 135 | Sinotrechiama yunnanus Belousov, Kabak & Liang, 2019 | Yunnan, Dayao County | surface-dwelling |
| 136 | Trechus aghiazicus Belousov & Kabak, 2019 | Xinjiang, Zhaosu County | surface-dwelling |
| 137 | T. cratocephalus Belousov & Kabak, 2019 | Xinjiang, Zhaosu County | surface-dwelling |
| 138 | T. saluki Belousov & Kabak, 2019 | Xinjiang, Xinyuan County | surface-dwelling |
| 139 | T. torgaut Belousov & Kabak, 2019 | Xinjiang, Hejing County | surface-dwelling |
| 140 | T. tsanmensis Belousov & Kabak, 2019 | Xinjiang, Xinyuan County | surface-dwelling |
References
- Fang, J.; Li, W.B.; Wang, X.H.; Tian, M.Y. New cavernicolous ground beetles from Anhui Province, China (Coleoptera, Carabidae, Trechini, Platynini). ZooKeys 2020, 923, 33–50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tian, M.Y.; Huang, X.L.; Li, C.L. Contribution to the knowledge of subterranean ground beetles from eastern Wuling Mountains, China (Coleoptera: Carabidae: Trechinae). Zootaxa 2021, 4926, 521–534. [Google Scholar] [CrossRef]
- Deuve, T.; Tian, M.Y.; Ran, J.C. Trois caraboidea remarquables de la réserve nationale de maolan, dans le guizhou méridional, chine (coleoptera, carabidae et trechidae). Revue Française d’Entomologie (N.S.) 1999, 21, 131–138. [Google Scholar]
- Barr, T.C.; Holsinger, J.R. Speciation in cave faunas. Annu. Rev. Ecol. Syst. 1985, 16, 313–337. [Google Scholar] [CrossRef]
- Faille, A.; Casale, A.; Ribera, I. Phylogenetic relationships of west Mediterranean troglobitic Trechini ground beetles (Coleoptera: Carabidae). Zool. Scr. 2011, 40, 282–295. [Google Scholar] [CrossRef] [Green Version]
- Jeannel, R. Faune de France. In Coléoptères Carabiques; Paul Lechevalier et Fils Publ: Paris, France, 1941; Volume 39, p. 571. [Google Scholar]
- Casale, A.; Vigna, T.A.; Juberthie, C. Coleoptera: Carabidae. In Encyclopadai Biospeologica, 3nd ed.; Juberthie, C., Decu, V., Eds.; Marinela Nazareanu et Violeta Berlescu: Bucharest, Romania, 1998; pp. 1047–1081. [Google Scholar]
- Moldovan, O.T. Beetles. In Encyclopedia of Caves, 2nd ed.; White, W.B., Culver, D.C., Eds.; Elsevier: Amsterdam, The Nederland, 2012; pp. 54–62. [Google Scholar]
- Adams, D.C.; Rohlf, F.J.; Slice, D.E. Geometric morphometrics: Ten years of progress following the ‘revolution’. Ital. J. Zool. 2004, 71, 5–16. [Google Scholar] [CrossRef] [Green Version]
- Adams, D.C.; Rohlf, F.J.; Slice, D.E. A field comes of age: Geometric morphometrics in the 21st century. Hystrix 2013, 24, 7–14. [Google Scholar]
- Bookstein, F.L. Biometrics, biomathematics and the morphometric synthesis. Bull. Math. Biol. 1996, 58, 313–365. [Google Scholar] [CrossRef]
- Corti, M. Geometric morphometrics: An extension of the revolution. Trends Ecol. Evol. 1993, 8, 302–303. [Google Scholar] [CrossRef]
- Bai, M.; Yang, X.K. Application of geometric morphometrics in biological researches. Chin. Bull. Entomol. 2007, 44, 143–147. [Google Scholar]
- Chen, J.Y.; Schopf, J.W.; Bottjer, D.J.; Zhang, C.Y.; Kudryavtsev, A.B.; Tripathi, A.B.; Wang, X.Q.; Yang, Y.H.; Gao, X.; Yang, Y. Raman spectra of a Lower Cambrian ctenophore embryo from southwestern Shaanxi, China. Proc. Natl. Acad. Sci. USA 2007, 104, 6289–6292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, H.D.; Bai, M.; Li, S.; Lu, Y.Y.; Ma, D.Y. A study of the three-dimensional morphological complexity of insect hindwing articulation based on four scarab species (Coleoptera: Scarabaeoidea). Acta Entomol. Sin. 2015, 58, 1322–1330. [Google Scholar]
- Cardini, A. Missing the third dimension in geometric morphometrics: How to assess if 2D images really are a good proxy for 3D structures? Hystrix 2014, 25, 73–81. [Google Scholar]
- Gould, F.D. To 3D or not to 3D, that is the question: Do 3D surface analyses improve the ecomorphological power of the distal femur in placental mammals? PLoS ONE 2014, 9, e91719. [Google Scholar] [CrossRef] [Green Version]
- Mutanen, M. Delimitation difficulties in species splits: A morphometric case study on the Euxoa tritici complex (Lepidoptera, Noctuidae). Syst. Entomol. 2005, 30, 632–643. [Google Scholar] [CrossRef]
- Polihronakis, M. Morphometric analysis of intraspecific shape variation in male and female genitalia of Phyllophaga hirticula (Coleoptera: Scarabaeidae: Melolonthinae). Ann. Entomol. Soc. Am. 2006, 99, 144–150. [Google Scholar] [CrossRef]
- Tatsuta, H.; Mizota, K.; Akimoto, S.I. Relationship between size and shape in the sexually dimorphic beetle Prosopocoilus inclinatus (Coleoptera: Lucanidae). Biol. J. Linn. Soc. 2004, 81, 219–233. [Google Scholar] [CrossRef]
- Pizzo, A.; Macagno, A.L.M.; Roggero, A.; Rolando, A.; Palestrini, C. Epipharynx shape as a tool to reveal differentiation patterns between insect sister species: Insights from Onthophagus taurus and O. illyricus (Insecta: Coleoptera: Scarabaeidae). Org. Divers. Evol. 2009, 9, 189–200. [Google Scholar] [CrossRef] [Green Version]
- Ge, D.Y.; Chesters, D.; Gomez-Zurita, J.; Zhang, L.J.; Yang, X.K.; Vogler, A.P. Anti-predator defence drives parallel morphological evolution in flea beetles. Proc. R. Soc. B Biol. Sci. 2011, 278, 2133–2141. [Google Scholar] [CrossRef] [Green Version]
- Palestrini, C.; Roggero, A.; Nova, L.K.H.; Giachino, P.M.; Rolando, A. On the evolution of shape and size divergence in Nebria (Nebriola) ground beetles (Coleoptera, Carabidae). Syst. Biodiver. 2012, 1477, 10–15. [Google Scholar]
- Bai, M.; Beutel, R.G.; Song, K.Q.; Liu, W.G.; Malqin, H.; Li, S.; Hu, X.Y.; Yang, X.K. Evolutionary patterns of hind wing morphology in dung beetles (Coleoptera: Scarabaeinae). Arthropod Struct. Dev. 2012, 41, 505–513. [Google Scholar] [CrossRef] [PubMed]
- Magniez-Jannin, F.; David, B.; Dommergues, J.L.; Su, Z.H.; Okada, T.S.; Osawa, S. Analysing disparity by applying combined morphological and molecular approaches to French and Japanese carabid beetles. Biol. J. Linn. Soc. 2000, 71, 343–358. [Google Scholar] [CrossRef]
- Garnier, S.; Magniez-Jannin, F.; Rasplus, J.Y.; Alibert, P. When morphometry meets genetics: Inferring the phylogeography of Carabus solieri using Fourier analyses of pronotum and male genitalia. J. Evolution. Biol. 2005, 18, 269–280. [Google Scholar] [CrossRef]
- Benítez, H.A.; Vidal, M.; Briones, R.; Jerez, V. Sexual dimorphism and morphological variation in populations of Ceroglossus chilensis (Eschscholtz, 1829) (Coleoptera, Carabidae). J. Entomol. Res. Soc. 2010, 12, 87–95. [Google Scholar]
- Benítez, H.A.; Lemic, D.; Bažok, R.; Gallardo-Araya, C.M. Evolutionary directional asymmetry and shape variation in Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae): An example using hind wings. Biol. J. Linn. Soc. 2014, 111, 110–118. [Google Scholar] [CrossRef] [Green Version]
- Roggero, A. Analysis of shape variation in Phalops Erichson genus (Coleoptera, Scarabaeoidea, Onthophagini). Ital. J. Zool. 2004, 71, 73–78. [Google Scholar] [CrossRef]
- Macagno, A.L.M.; Pizzo, A.; Roggero, A.; Palestrini, C. Horn polyphenism and related head shape variation in a single-horned dung beetle: Onthophagus (Palaeonthophagus) fracticornis (Coleoptera: Scarabaeidae). J. Zool. Syst. Evol. Res. 2009, 47, 96–102. [Google Scholar] [CrossRef]
- Bai, M.; Beutel, R.G.; Shih, C.K.; Ren, D.; Yang, X.K. Septiventeridae, a new and ancestral fossil family of Scarabaeoidea (Insecta: Coleoptera) from the Late Jurassicto Early Cretaceous Yixian Formation. J. Syst. Palaeontol. 2013, 11, 359–374. [Google Scholar] [CrossRef]
- Růžička, J.; Schneider, J.; Qubaiova, J.; Nishikawa, M. Revision of Palaearctic and Oriental Necrophila Kirby & Spence, part 2: Subgenus Chrysosilpha Portevin (Coleoptera: Silphidae). Zootaxa 2012, 3360, 33–58. [Google Scholar]
- Zinetti, F.; Dapporto, L.; Vanni, S.; Magrini, P.; Bartolozzi, L.; Chelazzi, G.; Ciofi, C. Application of molecular genetics and geometric morphometrics to taxonomy and conservation of cave beetles in central Italy. J. Insect Conserv. 2013, 17, 921–932. [Google Scholar] [CrossRef]
- Uéno, S.I. New Sinaphaenops (Coleoptera, Trechinae) from Southern Guizhou, with Notes on Thaumastaphaenops pulcherrimus. Elytra 2002, 30, 57–72. [Google Scholar]
- Uéno, S.I. Notes on Guizhaphaenops (Coleoptera, Trechinae), with Descriptions of Two New Species. Elytra 2000, 28, 247–264. [Google Scholar]
- Uéno, S.I. New Cave Trechines (Coleoptera, Trechinae) from Northeastern Guizhou, South China. J. Spel. Soc. Jpn. 2000, 25, 1–38. [Google Scholar]
- Deuve, T.; Tian, M.Y. Trois nouveaux Trechidae troglobies anophtalmes des karsts du Guizhou et du Zhejiang, en Chine (Coleoptera, Caraboidea). Bull. Soc. Entomol. France 2015, 102, 397–402. [Google Scholar]
- Tian, M.Y.; Chen, M.Z.; Ma, Z.J. A new anophthalmic trechine genus and two new species from southern Guizhou, China (Coleoptera: Carabidae: Trechini). Zootaxa 2020, 4766, 575–587. [Google Scholar] [CrossRef]
- Tian, M.Y.; Yin, H.M.; Huang, S.B. Du’an Karst of Guangxi: A kingdom of the cavernicolous genus Dongodytes Deuve (Coleoptera: Carabidae: Trechinae). ZooKeys 2014, 454, 69–107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tian, M.Y.; Huang, S.B.; Wang, X.H.; Tang, M.R. Contributions to the knowledge of subterranean trechine beetles in southern China’s karsts: Five new genera (Insecta: Coleoptera: Carabidae: Trechini). ZooKeys 2016, 564, 121–156. [Google Scholar] [CrossRef] [Green Version]
- Tian, M.Y.; Huang, S.B.; Wang, D.M. Discovery of a most remarkable cave-specialized trechine beetle from southern China (Coleoptera, Carabidae, Trechinae). ZooKeys 2017, 2017, 37–47. [Google Scholar] [CrossRef] [Green Version]
- Uéno, S.I. Two New Cave Trechines (Coleoptera, Trechinae) from Western Zhejiang, East China. J. Spel. Soc. Jpn. 2007, 32, 9–22. [Google Scholar]
- Belousov, I.A.; Kabak, I.I. New species of the genus Trechus Clairville, 1806 from the Chinese Tien Shan (Coleoptera: Carabidae). Zootaxa 2019, 4679, 47–68. [Google Scholar] [CrossRef] [PubMed]
- Belousov, I.A.; Kabak, I.I.; Liang, H.B. New species of the tribe Trechini from China (Coleoptera: Carabidae). Zootaxa 2019, 4656, 143–152. [Google Scholar] [CrossRef] [PubMed]
- Rohlf, F.J. tpsUtil, file Utility Program, version 1.64; Department of Ecology and Evolution, State University of New York at Stony Brook: Stony Brook, NY, USA, 2013; Available online: http://sbmorphometrics.org/ (accessed on 12 September 2019).
- Rohlf, F.J. The Tps Series of Software. Hystrix Ital. J. Mamm. 2015, 26, 9–12. [Google Scholar]
- Bookstein, F.L. Thin-plate splines and the atlas problem for biomedical images. In Proceedings of the 12th International Conference on Information Processing in Medical Imaging, Berlin/Heidelberg, Germany, 7–12 July 1991; Colchester, A.C.F., Hawkes, D.J., Eds.; Springer: Berlin, Germany, 1991; pp. 326–342. [Google Scholar]
- Rohlf, F.J.; Bookstein, F.L. Computing the uniform component of shape variation. Syst. Biol. 2003, 52, 66–69. [Google Scholar] [CrossRef] [PubMed]
- Rohlf, F.J. On the use of shape spaces to compare morphometric methods. Hystrix Ital. J. Mamm. 2000, 11, 9–25. [Google Scholar]
- Deuve, T. Deux remarquables Trechinae anophtalmes des cavités souterraines du Guangxi nord-occidental, Chine (Coleoptera, Trechidae). Bull. Soc. Entomol. France. 2002, 107, 515–523. [Google Scholar]
- Howarth, F.G. Ecology of cave arthropods. Annu. Rev. Entomol. 1983, 28, 365–389. [Google Scholar] [CrossRef]
- Moldovan, O.T.; Jalžić, B.; Erichsen, E. Adaptation of the mouthparts in some subterranean Cholevinae (Coleoptera, Leiodidae). Natura Croatica 2004, 13, 1–18. [Google Scholar]
- White, W.; Culver, D.C. Encyclopedia of Caves; Academic Press: Amsterdam, The Nederland, 2012; p. 945. [Google Scholar]
- Forsythe, T.G. The relationship between body form and habit in some Carabidae (Coleoptera). J. Zool. 1987, 211, 643–666. [Google Scholar] [CrossRef]
- Pipan, T.; Culver, D.C. Shallow subterranean habitats. In Encyclopedia of Caves, 2nd ed.; White, W., Culver, D.C., Eds.; Academic Press: Amsterdam, The Nederland, 2012; pp. 683–690. [Google Scholar]
- Liu, W.X.; Golovatch, S.I.; Wesner, T.; Tian, M.Y. Convergent Evolution of Unique Morphological Adaptations to a Subterranean Environment in Cave Millipedes (Diplopoda). PLoS ONE 2017, 12, e0170717. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, X.Z.; Wipfler, B.; Ribera, I.; Liang, H.B.; Tian, M.Y.; Ge, S.Q.; Beutel, R.G. The cephalic morphology of free-living and cave-dwelling species of trechine ground beetles from China (Coleoptera, Carabidae). Org. Divers. Evol. 2018, 18, 125–142. [Google Scholar] [CrossRef]
- Luo, X.Z.; Wipfler, B.; Ribera, I.; Liang, H.B.; Tian, M.Y.; Ge, S.Q.; Beutel, R.G. The thoracic morphology of cave-dwelling and free-living ground beetles from China (Coleoptera, Carabidae, Trechinae). Arthropod Struct. Dev. 2018, 47, 662–674. [Google Scholar] [CrossRef]
- Luo, X.Z.; Antunes-Carvalho, C.; Ribera, I.; Beutel, R.G. The thoracic morphology of the troglobiontic cholevine species Troglocharinus ferreri (Coleoptera, Leiodidae). Arthropod Struct. Dev. 2019, 53, 100900. [Google Scholar] [CrossRef] [PubMed]
- Tian, M.Y. New records and new species of cave-dwelling trechine beetles from Mulun Nature Reserve, northern Guangxi, China (Insecta: Coleoptera: Carabidae: Trechinae). Subterr. Biol. 2019, 7, 69–73. [Google Scholar]
- Tian, M.Y.; Huang, S.B. Contribution to the knowledge of the cavernicolous beetle genus Aspidaphaenops Uéno from Guizhou (Coleoptera: Carabidae: Trechinae). Zootaxa 2018, 4422, 244–258. [Google Scholar] [CrossRef]
- Tian, M.Y. New records and a new species of the cavernicolous genus Guiodytes Tian, 2013 from Guangxi, China (Coleoptera: Carabidae: Scaritinae). Zootaxa 2014, 3861, 355–362. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lin, W.; Tian, M.Y. Supplemental notes on the genus Libotrechus Uéno, with description of a new species from Guangxi, southern China (Coleoptera: Carabidae: Trechinae). Coleopts Bull. 2014, 68, 429–433. [Google Scholar] [CrossRef]
- Deuve, T.; He, L.; Tian, M.Y. Descriptions of the first semi-aphenopsian troglobiotic Patrobini and of a new anophthalmic cave-dwelling Trechini from central Sichuan, China (Coleoptera: Caraboidea). Ann. Soc. Entomol. France 2020, 37, 1–13. [Google Scholar] [CrossRef]
- Pang, J.M.; Tian, M.Y. A remarkably modified species of the tribe Platynini (Coleoptera, Carabidae) from a limestone cave in Jiangxi Province, eastern China. ZooKeys 2014, 382, 1–12. [Google Scholar]
- Wizen, G.; Gasith, A. An unprecedented role reversal: Ground beetle larvae (Coleoptera: Carabidae) lure amphibians and prey upon them. PLoS ONE 2011, 6, e25161. [Google Scholar] [CrossRef] [Green Version]
- Sugiura, S.; Sato, T. Successful escape of bombardier beetles from predator digestive systems. Biol. Lett. 2018, 14, 20170647. [Google Scholar] [CrossRef] [Green Version]
- Huang, S.B. Molecular Phylogeny of the Cavernicolous Trechine Beetles in China (Coleoptera: Carabidae). Master’s Thesis, South China Agricultural University, Guangzhou, China, 2016. [Google Scholar]
- Huang, S.B.; Tian, M.Y.; Faille, A. A preliminary phylogeny of cave trechine beetles from China (Coleoptera: Carabidae: Trechini). ARPHA Conf. Abstr. 2020, 3, e51897. [Google Scholar] [CrossRef]
- Faille, A.; Ribera, I.; Deharveng, L.; Bourdeau, C.; Garnery, L.; Deuve, T. A molecular phylogeny shows the single origin of the Pyrenean subterranean Trechini ground beetles (Coleoptera: Carabidae). Mol. Phylogenet. Evol. 2010, 54, 97–106. [Google Scholar] [CrossRef] [PubMed]
Figure 1.
Morphological characteristics of four different adaptive types of ground beetles. (a) Surface-dwelling (Sinotrechiama yunnanus); (b) anophthalmic (Sinotroglodytes yanwangi); (c) semi-aphaenopsian (Aspidaphaenops dudou); and (d) aphaenopsian (Giraffaphaenops clarkei).
Figure 1.
Morphological characteristics of four different adaptive types of ground beetles. (a) Surface-dwelling (Sinotrechiama yunnanus); (b) anophthalmic (Sinotroglodytes yanwangi); (c) semi-aphaenopsian (Aspidaphaenops dudou); and (d) aphaenopsian (Giraffaphaenops clarkei).
Figure 2.
Landmark and semilandmark configurations of ground beetle specimens. (a) The right side of the head (50 positions); (b) right side of the pronotum (50 positions); and (c) right side of the elytra (56 positions).
Figure 2.
Landmark and semilandmark configurations of ground beetle specimens. (a) The right side of the head (50 positions); (b) right side of the pronotum (50 positions); and (c) right side of the elytra (56 positions).
Figure 3.
Principal component analysis (PCA) of four different adaptive types of ground beetles: (a,b) head; (c,d) pronotum; (e,f) elytra. (a,c,e) represent scatterplot; (b,d,f) represent the energy map.
Figure 3.
Principal component analysis (PCA) of four different adaptive types of ground beetles: (a,b) head; (c,d) pronotum; (e,f) elytra. (a,c,e) represent scatterplot; (b,d,f) represent the energy map.
Figure 4.
Phenotypic tree of ground beetle genera based on the Procrustes distance. (a) Head, (b) pronotum, (c) elytra, and (d) integrated morphology. Anphaenopsian: red letters; semi-anphaenopsian: green letters; anophthalmic: blue letters; surface-dwelling: purple letters.
Figure 4.
Phenotypic tree of ground beetle genera based on the Procrustes distance. (a) Head, (b) pronotum, (c) elytra, and (d) integrated morphology. Anphaenopsian: red letters; semi-anphaenopsian: green letters; anophthalmic: blue letters; surface-dwelling: purple letters.
Table 1.
Mahalanobis distances from four adaptive types of ground beetles based on the head, pronotum, and elytra, respectively.
Table 1.
Mahalanobis distances from four adaptive types of ground beetles based on the head, pronotum, and elytra, respectively.
| Aphaenopsian | Semi-Aphaenopsian | Anophthalmic | |
|---|---|---|---|
| Semi-aphaenopsian | 11.1596//8.9433//12.6030 | ||
| Anophthalmic | 13.9436//10.7282//15.3457 | 6.6324//7.6456//7.0232 | |
| Surface-dwelling | 28.5719//20.8313//20.7926 | 23.0163//16.3761//18.8595 | 22.5005//16.7463//16.2172 |
Table 2.
Procrustes distances from four adaptive types of ground beetles based on the head, pronotum, and elytra, respectively.
Table 2.
Procrustes distances from four adaptive types of ground beetles based on the head, pronotum, and elytra, respectively.
| Aphaenopsian | Semi-Aphaenopsian | Anophthalmic | |
|---|---|---|---|
| Semi-aphaenopsian | 0.1319//0.1409//0.0516 | ||
| Anophthalmic | 0.2451//0.2342//0.0854 | 0.1227//0.0995//0.0485 | |
| Surface-dwelling | 0.3429//0.3258//0.1032 | 0.2275//0.1981//0.0644 | 0.109//0.101//0.0589 |
Table 3.
P-values of the differences in Mahalanobis and Procrustes distances for the four adaptive types of ground beetles (10,000 permutation test, consistent for the head, pronotum, and elytra).
Table 3.
P-values of the differences in Mahalanobis and Procrustes distances for the four adaptive types of ground beetles (10,000 permutation test, consistent for the head, pronotum, and elytra).
| Aphaenopsian | Semi-Aphaenopsian | Anophthalmic | |
|---|---|---|---|
| Semi-aphaenopsian | <0.0001 | ||
| Anophthalmic | <0.0001 | <0.0001 | |
| Surface-dwelling | <0.0001 | <0.0001 | <0.0001 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Chen, M.; Guo, W.; Huang, S.; Luo, X.; Tian, M.; Liu, W. Morphological Adaptation of Cave-Dwelling Ground Beetles in China Revealed by Geometric Morphometry (Coleoptera, Carabidae, Trechini). Insects 2021, 12, 1002. https://doi.org/10.3390/insects12111002
AMA Style
Chen M, Guo W, Huang S, Luo X, Tian M, Liu W. Morphological Adaptation of Cave-Dwelling Ground Beetles in China Revealed by Geometric Morphometry (Coleoptera, Carabidae, Trechini). Insects. 2021; 12(11):1002. https://doi.org/10.3390/insects12111002
Chicago/Turabian StyleChen, Mengzhen, Wanru Guo, Sunbin Huang, Xiaozhu Luo, Mingyi Tian, and Weixin Liu. 2021. "Morphological Adaptation of Cave-Dwelling Ground Beetles in China Revealed by Geometric Morphometry (Coleoptera, Carabidae, Trechini)" Insects 12, no. 11: 1002. https://doi.org/10.3390/insects12111002
Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.
