Research Article |
Corresponding author: L. Lee Grismer ( lgrismer@lasierra.edu ) Academic editor: Uwe Fritz
© 2021 L. Lee Grismer, Hai Ngoc Ngo, Shuo Qi, Ying-Yong Wang, Minh Duc Le, Thomas Ziegler.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Grismer LL, Ngo HN, Qi S, Wang Y-Y, Le MD, Ziegler T (2021) Phylogeny and evolution of habitat preference in Goniurosaurus (Squamata: Eublepharidae) and their correlation with karst and granite-stream-adapted ecomorphologies in species groups from Vietnam. Vertebrate Zoology 71: 335-352. https://doi.org/10.3897/vz.71.e65969
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Abstract
Maximum likelihood (ML) and Bayesian inference (BI) analyses using two mitochondrial (16S and cyt b) and two nuclear (CMOS and RAG1) genes and 103 specimens recovered the first phylogenies of all 23 extant species of Goniurosaurus. The analyses strongly supported the recognition of four monophyletic species groups with identical inter-specific relationships within the kuroiwae, lichtenfelderi, and yingdeensis groups but discordant topologies at some nodes within the luii group. Both analyses recovered a polyphyletic G. luii with respect to G. kadoorieorum, and owing to the lack of diagnostic characters in the latter, it is considered a junior synonym of G. luii. A stochastic character mapping analysis of karst versus non-karst habitat preference suggested that karstic landscapes may have played a major role in the evolution and diversification of Goniurosaurus. A karst habitat preference is marginally supported as the most probable ancestral condition for Goniurosaurus as well as for the kuroiwae, luii, and yingdeensis groups. However, a non-karst habitat preference is marginally supported as the most probable ancestral condition for the lichtenfelderi group. Multivariate and univariate ecomorphological analyses of the karst-adapted G. catbaensis, G. huuliensis, and G. luii of the luii group and the granite-stream-adapted G. lichtenfelderii of the lichtenfelderi group demonstrated that their markedly statistically different body shapes may be an adaptive response that contributes to habitat partitioning in areas of northern Vietnam where they are nearly sympatric.
Asia, stochastic character mapping, systematics, synonymy, tiger geckos
Eublepharid geckos of the genus Goniurosaurus Barbour, 1908 comprise 23 saxicolous specialists (Uetz et al. 2021) that extend from the Ryukyu Archipelago in Japan, southward through East Asia to northern Vietnam. Goniurosaurus is a well-defined monophyletic group (
In an effort to continue building a more global understanding of the phylogenetic relationships within Goniurosaurus, we expanded the mito-nuclear data set of
Species and GenBank accession numbers of the sequenced specimens used herein.
Species/Specimen | 16s | cytb | CMOS | RAG1 |
---|---|---|---|---|
Goniurosaurus araneus | AB308460 | |||
G. araneus ECNU-V0008 | MT533259 | |||
G. araneus JFBM15830 | HQ426537 | HQ426286 | ||
G. bawanglingensis BL-RBZ-021 | MH247190 | MH247201 | MH247212 | MH247223 |
G. bawanglingensis BL-RBZ-022 | MH247191 | MH247202 | MH247213 | MH247224 |
G. bawanglingensis BL-RBZ-023 | MH247192 | MH247203 | MH247214 | MH247225 |
G. bawanglingensis BL-RBZ-024 | MH247193 | MH247204 | MH247215 | MH247226 |
G. bawanglingensis SYS r002162 | MT995758 | MT995773 | ||
G. catbaensis G33 | MW741550 | MW650944 | ||
G. catbaensis G34 | MW741551 | MW650945 | ||
G. catbaensis G35 | MW650946 | |||
G. catbaensis MHNG 2699.49 | EU499389 | |||
G. gezhi ECNU-V0038 | MT533260 | |||
G. gezhi ECNU-V0040 | MT533261 | |||
G. gezhi ECNU-V0042 | MT533262 | |||
G. gezhi ECNU-V0046 | MT533263 | |||
G. gezhi ECNU-V0047 | MT533264 | |||
G. gollum SYS r002420 | MT995784 | MT995787 | MW727559 | MW727594 |
G. gollum SYS r002421 | MT995785 | MT995788 | MW727560 | MW727595 |
G. gollum SYS r002422 | MT995786 | MT995789 | MW727561 | MW727596 |
G. hainanensis BL-RBZ-041 | MH247194 | MH247205 | MH247216 | MH247227 |
G. hainanensis BL-RBZ-042 | MH247195 | MH247206 | MH247217 | MH247228 |
G. hainanensis SYS r000349 | KC765080 | |||
G. hainanensis JK1 | AB308458 | |||
G. huuliensis Gohu | AB853453 | AB853479 | ||
G. huuliensis G21 | MW650936 | |||
G. huuliensis G23 | MW650937 | |||
G. huuliensis G24 | MW650938 | |||
G. kadoorieorum ECNU-V0058 | MT533258 | |||
G. kadoorieorum ECNU-V0060 | MT533265 | |||
G. kadoorieorum ECNU-V0061 | MT533266 | |||
G. kuroiwae Goku1 Northern Okinawa | AB853448 | AB853473 | ||
G. kuroiwae Goku2 Southern Okinawa | AB853445 | |||
G. kuroiwae Goor1 Southern Okinawa | AB853446 | AB853467 | ||
G. kwanghua ECNU-V0003 | MK782788 | MK782782 | MK782776 | MK782770 |
G. kwanghua ECNU-V0004 | MK782789 | MK782783 | MK782777 | MK782771 |
G. kwanghua ECNU-V0005 | MK782790 | MK782784 | MK782778 | MK782772 |
G. kwangsiensis ECNU-V0009 | MK782786 | MK782780 | MK782774 | MK782768 |
G. liboensis SYS r000217 | KC900230 | |||
G. lichtenfelderii ECNU-V0007 | MK782785 | MK782779 | MK782773 | MK782767 |
G. lichtenfelderii IEBR 3692 | JF799756 | |||
G. luii ECNU-V0012 | MK782787 | MK782781 | MK782775 | MK782769 |
G. luii Golu2 | EF081254 | |||
G. luii Golu3 | AB853452 | AB853478 | ||
G. luii SYSr 000255 | KC765083 | |||
G. luii SYSr 000256 | KC765084 | |||
G. luii ZFMK 87057 | EU499391 | |||
G. luii TG00795 | HQ426287 | |||
G. orientalis Goku3 | AB853446 | |||
G. orientalis Goor2 | AB853443 | AB853461 | ||
G. orientalis Goor3 | AB853462 | |||
G. sengokui Gose1 | AB853444 | AB853463 | ||
G. sengokui Gose2 | AB853464 | |||
G. sengokui KUZ 62087 | HQ876393 | |||
G. splendens Gosp1 | AB853451 | AB853477 | ||
G. splendens Gosp2 | AB853449 | |||
G. splendens Gosp3 | AB853450 | |||
G. toyamai Goto1 | AB853447 | AB853468 | ||
G. toyamai Goto2 | AB853469 | |||
G. variusi SYS r002331 | MT995754 | MT995769 | MW727556 | MW727590 |
G. variusi SYS r002332 | MT995755 | MT995770 | ||
G. variusi SYS r002333 | MT995753 | MT995768 | ||
G. variusi SYS r002362 | MT995756 | MT995771 | MW727557 | MW727592 |
G. variusi SYS r002363 | MT995757 | MT995772 | MW727558 | MW727593 |
G. variusi SYS r002485 | MW721828 | MW727532 | MW727562 | MW727597 |
G. variusi SYS r002486 | MW721829 | MW727533 | MW727563 | MW727598 |
G. yamashinae Goya1 | AB853442 | AB853460 | ||
G. yamashinae Goya2 | AB853441 | AB853459 | ||
G. yamashinae Goya3 | AB853458 | |||
G. yingdeensis Field number DYA01 | MW721830 | MW727534 | MW727574 | MW727605 |
G. yingdeensis Field number DYA02 | MW721831 | MW727535 | MW727575 | MW727606 |
G. yingdeensis Field number HS01 | MW721832 | MW727536 | MW727576 | MW727607 |
G. yingdeensis Field number HS02 | MW721833 | MW727537 | MW727577 | MW727608 |
G. yingdeensis Field number LT01 | MW721834 | MW727538 | MW727580 | MW727611 |
G. yingdeensis Field number LT02 | MW721835 | MW727539 | MW727581 | MW727612 |
G. yingdeensis SYS r000549 | KC765082 | |||
G. yingdeensis SYS r000550 | KC900231 | |||
G. yingdeensis SYS r001271 | MT995759 | MT995774 | MW727547 | |
G. yingdeensis SYS r001272 | MT995760 | MT995775 | MW727548 | |
G. yingdeensis SYS r001493 | MT995761 | MT995776 | MW727551 | |
G. yingdeensis SYS r0002115 | MT995762 | MT995777 | ||
G. zhelongi Field number HW01 | MW721838 | MW727540 | MW727578 | MW727609 |
G. zhelongi Field number HW02 | MW721839 | MW727541 | MW727579 | MW727610 |
G. zhelongi Field number MDA01 | MW721836 | MW727542 | MW727582 | MW727613 |
G. zhelongi Field number MDA02 | MW721837 | MW727543 | MW727583 | MW727614 |
G. zhelongi Field number TZ01 | MW721840 | MW727544 | MW727584 | MW727615 |
G. zhelongi Field number TZ02 | MW721841 | MW727545 | MW727585 | MW727616 |
G. zhelongi SYS r000816 | KJ423105 | MT995778 | MW727570 | |
G. zhelongi SYS r001491 | MT995763 | MT995779 | MW727549 | |
G. zhelongi SYS r001492 | MT995764 | MT995780 | MW727550 | |
G. zhelongi SYS r002108 | MT995765 | MT995781 | ||
G. zhoui BL-RBZ-001 | MH247196 | MH247207 | MH247218 | MH247229 |
G. zhoui BL-RBZ-004 | MH247197 | MH247208 | MH247219 | MH247230 |
G. zhoui BL-RBZ-006 | MH247198 | MH247209 | MH247220 | MH247231 |
G. zhoui BL-RBZ-007 | MH247199 | MH247210 | MH247221 | MH247232 |
G. zhoui BL-RBZ-008 | MH247200 | |||
G. zhoui SYS r002213 | MT995766 | MT995782 | MW727553 | |
G. zhoui SYS r002214 | MT995767 | MT995783 | MW727554 | |
Eublepharis macularius | AB853454 | AB853480 |
Genomic DNA was extracted from muscle tissue samples, using a DNA extraction kit from Tiangen Biotech (Beijing) Co., Ltd. Primers used for 16S were r16S-5L (5’- GGTMMYGCCTGCCCAGTG -3’) and 16Sbr-H (5’- CCGGTCTGAACTCAGATCACGT-3’) (
We constructed Maximum Likelihood (ML), Bayesian Inference (BI), and Bayesian Evolutionary Analysis by Sampling Trees (BEAST) phylogenetic trees using a concatenated data set composed of 3070 base pairs (bp) of the mitochondrial genes, 16S (633 bp) and cyt b (1075 bp), and the nuclear genes, CMOS (472 bp) and RAG1 (890), from 103 specimens of 23 species of Goniurosaurus with varying degrees of sequence coverage across the samples (Table
A Maximum likelihood (ML) analysis partitioned by gene was implemented using the IQ-TREE webserver (
An input file was constructed in Bayesian Evolutionary Analysis Utility (BEAUti) v. 2.4.6 using a relaxed lognormal clock with unlinked site models, linked trees and clock models, and a Yule prior and run in BEAST on CIPRES (Cyberinfrastructure for Phylogenetic Research;
The BEAST tree was converted to newick format and pruned using the drop.tip () command (
The coding of habitat preference for each species was determined from the literature and field observations of the authors (Table
Species | 1° habitat | 2° habitat | Source |
kuroiwae group | |||
G. splendens | karst | forest | Nakamura and Ueno (1963), H. Ota pers. comm., L. Grismer pers. obs. |
G. toyamai | forest | H. Ota pers. comm. | |
G. kuroiwae North | forest | H. Ota pers. comm., L. Grismer pers. obs., | |
G. kuroiwae South | karst | forest | Nakamura and Ueno (1963), H. Ota pers. comm., L. Grismer pers. obs. |
G. yamashinae | karst | forest | H. Ota pers. comm., L. Grismer pers. obs., |
G. sengokui | karst | forest | Werner et al. (2004), H. Ota pers. comm. |
G. orientalis | karst | H. Ota pers. comm. | |
yingdeensis group | |||
G. gollum | karst |
|
|
G. yingdeensis | karst | granite | Wang et al. (2010), S. Qi pers. obs. |
G. zhelongi | karst | granite | S. Qi, pers. obs., Wang et al. (2014) |
G. variusi | karst |
|
|
lichtenfelderi group | |||
G. bawanglingensis | granite | karst | Grismer et al. (2002), |
G. zhoui | karst | granite |
|
G. kwanghua | karst | granite | Zhu et al. (2020) |
G. lichtenfelderii | granite |
|
|
G. hainanensis | granite | volcanic | S. Qi pers. obs., L. Grismer pers. obs. |
luii group | |||
G. catbaensis | karst |
|
|
G. gezhi | karst | Zhu et al. (2020) | |
G. araneus | karst |
|
|
G. kadoorieorum | karst |
|
|
G. huuliensis | karst |
|
|
G. luii | karst |
|
|
G. liboensis | karst |
|
|
G. kwangsiensis | karst |
|
An ecomorphological analysis was conducted using four of the five recorded species from Vietnam (
Measurements were taken with dial calipers to the nearest 0.1 mm on the right side of each individual. Abbreviations are as follows: snout-vent length (SVL), from tip of snout to vent; axilla to groin length (AG), from posterior edge of forelimb insertion to anterior edge of hind limb insertion; maximum body width (BW), greatest width of torso, taken at level of midbody; maximum body height (BH), from dorsal surface of body to belly; internarial distance (ID), distance between nares; head length (HL), from the tip of snout to posterior edge of occiput; maximum head width (HW); cheek height (CH), from posterior edge of labial to top of head at parietal region; interorbital distance (IO), distance between posteriormost points of eyes; diameter of auditory meatus (AD); snout to eye distance (SL), measured from tip of snout to anteriormost point of eye; diameter of eye (ED), greatest diameter of eye; eye to ear distance (EE), from posterior margin of eye to posterior margin of ear; forelimb length (FLL), from axilla to the tip of the fourth finger; hind limb length (HLL), from groin to the tip of the fourth toe. To remove potential effects of allometry, size was adjusted using the following equation: Xadj=log(X)-β[log(SVL)-log(SVLmean)], where Xadj=adjusted value; X=measured value; β=unstandardized regression coefficient for each population; and SVLmean=overall average SVL of all populations (
An analysis of variance (ANOVA) was performed on a data set coded for species to search for the presence of statistically significant mean differences (p < 0.05) among characters across the selected subset of species in the luii and lichtenfelderi groups. Character means bearing statistical differences among species were subjected to a TukeyHSD test to ascertain which species pairs differed significantly from each other for those particular characters. A Student t-test was also performed on a second data set coded for only habitat preference (karst versus non-karst) to search for the presence of statistically significant mean differences (p < 0.05) among the same subsets of species coded for habitat. Violin plots with inserted boxplots were generated in order to visualize the range, frequency, mean, 50% quartile, and degree of differences between the dependent variables for both data sets bearing statistically different mean values.
The morphospatial clustering of the two separate data sets (species and habitat preference) were visualized using principal component analysis (PCA) along the ordination of the first two principal components (PC) using the Adegenet package in R (Jombart et al. 2010) and implemented by the prcomp () command. The data were log-transformed prior to analysis in order to normalize their distribution so as to ensure characters with very large or very low values could not over-leverage the results owing to intervariable nonlinearity. All statistical analyses were performed using R.3.1.2 (
The ML, BI, and BEAST analyses recovered strong nodal support (UFB 98–100/BPP 1.00) for the monophyly of all four species groups with the kuroiwae group being the strongly supported (100/1.00) sister group to the remaining three groups (Fig.
Mito-nuclear maximum likelihood topology with ultrafast bootstrap values (UFB) and Bayesian posterior probabilities (BPP) at the nodes. All species except Goniurosaurus luii had strong nodal support (100/1.00) for their monophyly. The inset in the luii species group is a section of the BI analysis showing the non-monophyly of G. luii with respect to G. kadoorieorum. Colored species are those used in the ecomorphological analyses.
The AICc scores for the three transition rate models of the SCM analysis were ARD = 34.547134 and SYM and ER = 32.099451. The SCM analysis using either the SYM or ER model suggests that a karst habitat preference is the most probable ancestral condition for Goniurosaurus (57.0% probability), the kuroiwae group (62.7%), the luii group (90.0%), and the yingdeensis group (95.7%; Fig.
In both the species and habitat preference PCA analyses, PC1 accounted for 49.1% of the variation in the data set and loaded most heavily for limb length (FLL and HLL), snout length (SL), eye diameter (ED), interorbital distance (IO), head width (HW), and head length (HL). PC2 accounted for an additional 13.3% of the variation and loaded most heavily for body width (BW) and body height (BH) (Figs
A. Principal component analysis of the karst-adapted species G. catbaensis, G. huuliensis, and G. luii of the luii group and the granite-stream-adapted G. lichtenfelderii of the lichtenfelderi group. B. Violin plots overlain with box plots showing the range, frequency, mean (white dot), and 50% quartile (black rectangle) of the size-adjusted morphometric characters.
The PCA analysis of the karst-adapted Goniurosaurus catbaensis, G. huuliensis, and G. luii of the luii group demonstrates that their body shapes greatly overlap in morphospace despite there being several slight, but statistically significant mean differences among them (Fig.
Difference, lower and upper ranges, and adjusted p values of statistically significant mean differences between species pairs for each character based on ANOVA and subsequent TukeyHSD analyses.
axilla-groin (AG) | difference | lower range | upper range | p adjusted |
huuliensis-catbaensis | 0.095633573 | 0.072292064 | 0.118975082 | 3.37E-10 |
lichtenfelderi-catbaensis | –0.075967576 | –0.094200659 | –0.057734493 | 3.37E-10 |
luii-catbaensis | –0.029676257 | –0.05225407 | –0.007098445 | 0.004206065 |
lichtenfelderi-huuliensis | –0.171601149 | –0.195246969 | –0.14795533 | 3.37E-10 |
luii-huuliensis | –0.12530983 | –0.152447204 | –0.098172456 | 3.37E-10 |
luii-lichtenfelderi | 0.046291319 | 0.023399042 | 0.069183596 | 1.60E-06 |
body width (BW) | ||||
huuliensis-catbaensis | 0.106179184 | 0.066412755 | 0.145945613 | 4.37E-10 |
lichtenfelderi-huuliensis | –0.083314667 | –0.123599543 | –0.043029791 | 8.67E-07 |
luii-huuliensis | –0.121548632 | –0.167781995 | –0.075315269 | 5.34E-10 |
body height (BH) | ||||
huuliensis-catbaensis | 0.094637915 | 0.046801122 | 0.142474708 | 2.84E-06 |
lichtenfelderi-huuliensis | –0.07317021 | –0.121630666 | –0.024709755 | 0.000647886 |
luii-huuliensis | –0.125013692 | –0.180629845 | –0.069397539 | 7.11E-08 |
luii-lichtenfelderi | –0.051843482 | –0.098759605 | –0.004927359 | 0.02359844 |
internarial distance (ID) | ||||
lichtenfelderi-catbaensis | –0.082396274 | –0.105742691 | –0.059049857 | 3.37E-10 |
luii-catbaensis | –0.076638786 | –0.105548379 | –0.047729192 | 4.74E-10 |
lichtenfelderi-huuliensis | –0.096677642 | –0.126954757 | –0.066400527 | 3.37E-10 |
luii-huuliensis | –0.090920154 | –0.125668004 | –0.056172303 | 5.78E-10 |
head length (HL) | ||||
huuliensis-catbaensis | 0.075818967 | 0.058801575 | 0.092836359 | 3.37E-10 |
lichtenfelderi-catbaensis | –0.162875997 | –0.176169033 | –0.149582961 | 3.37E-10 |
luii-catbaensis | –0.029098886 | –0.045559496 | –0.012638276 | 3.82E-05 |
lichtenfelderi-huuliensis | –0.238694964 | –0.255934217 | –0.221455712 | 3.37E-10 |
luii-huuliensis | –0.104917853 | –0.124702663 | –0.085133043 | 3.37E-10 |
luii-lichtenfelderi | 0.133777111 | 0.117087238 | 0.150466985 | 3.37E-10 |
head width (HW) | ||||
huuliensis-catbaensis | 0.036775074 | 0.019138869 | 0.05441128 | 6.89E-07 |
lichtenfelderi-catbaensis | –0.158637831 | –0.172414249 | –0.144861413 | 3.37E-10 |
luii-catbaensis | –0.065002064 | –0.082061241 | –0.047942887 | 3.37E-10 |
lichtenfelderi-huuliensis | –0.195412905 | –0.213279039 | –0.177546772 | 3.37E-10 |
luii-huuliensis | –0.101777138 | –0.122281395 | –0.081272881 | 3.37E-10 |
luii-lichtenfelderi | 0.093635767 | 0.07633899 | 0.110932545 | 3.37E-10 |
head height (HH) | ||||
huuliensis-catbaensis | 0.108413032 | 0.073172094 | 0.143653969 | 3.37E-10 |
lichtenfelderi-catbaensis | –0.032237965 | –0.059766217 | –0.004709713 | 0.014142658 |
lichtenfelderi-huuliensis | –0.140650997 | –0.176351381 | –0.104950613 | 3.37E-10 |
luii-huuliensis | –0.14002168 | –0.180993602 | –0.099049757 | 3.37E-10 |
cheek height (CH) | ||||
huuliensis-catbaensis | 0.069595379 | 0.028246161 | 0.110944597 | 0.000101199 |
lichtenfelderi-catbaensis | –0.14807373 | –0.180373429 | –0.11577403 | 3.37E-10 |
luii-catbaensis | –0.057345812 | –0.09734215 | –0.017349473 | 0.001381599 |
lichtenfelderi-huuliensis | –0.217669109 | –0.259557409 | –0.175780808 | 3.37E-10 |
luii-huuliensis | –0.126941191 | –0.175014741 | –0.078867641 | 5.00E-10 |
luii-lichtenfelderi | 0.090727918 | 0.050174509 | 0.131281326 | 8.27E-08 |
interorbital distance (ID) | ||||
huuliensis-catbaensis | 0.05692565 | 0.034698839 | 0.079152461 | 9.29E-10 |
lichtenfelderi-catbaensis | –0.211451872 | –0.228814215 | –0.194089528 | 3.37E-10 |
luii-catbaensis | –0.03636425 | –0.057863835 | –0.014864664 | 9.22E-05 |
lichtenfelderi-huuliensis | –0.268377522 | –0.29089411 | –0.245860933 | 3.37E-10 |
luii-huuliensis | –0.093289899 | –0.1191313 | –0.067448499 | 3.37E-10 |
luii-lichtenfelderi | 0.175087622 | 0.15328859 | 0.196886655 | 3.37E-10 |
snout length (SL) | ||||
huuliensis-catbaensis | 0.108547374 | 0.083797596 | 0.133297152 | 3.37E-10 |
lichtenfelderi-catbaensis | –0.20706889 | –0.226402034 | –0.187735746 | 3.37E-10 |
lichtenfelderi-huuliensis | –0.315616264 | –0.340688712 | –0.290543816 | 3.37E-10 |
luii-huuliensis | –0.125435452 | –0.154210112 | –0.096660792 | 3.37E-10 |
luii-lichtenfelderi | 0.190180812 | 0.16590737 | 0.214454254 | 3.37E-10 |
ear diameter (ED) | ||||
huuliensis-catbaensis | –0.137477526 | –0.199198043 | –0.075757008 | 9.51E-08 |
lichtenfelderi-catbaensis | –0.338691314 | –0.386903935 | –0.290478693 | 3.37E-10 |
luii-catbaensis | –0.365692271 | –0.425393393 | –0.305991149 | 3.37E-10 |
lichtenfelderi-huuliensis | –0.201213788 | –0.263738975 | –0.138688602 | 3.37E-10 |
luii-huuliensis | –0.228214745 | –0.299972435 | –0.156457055 | 3.37E-10 |
eye to ear distance (EE) | ||||
huuliensis-catbaensis | 0.085091637 | 0.059731157 | 0.110452117 | 3.37E-10 |
lichtenfelderi-huuliensis | –0.06878479 | –0.094475902 | –0.043093678 | 4.25E-10 |
luii-huuliensis | –0.101777804 | –0.131262479 | –0.072293128 | 3.37E-10 |
luii-lichtenfelderi | –0.032993014 | –0.057865404 | –0.008120623 | 0.00377334 |
eye diameter (ED) | ||||
huuliensis-catbaensis | 0.085091637 | 0.059731157 | 0.110452117 | 3.37E-10 |
lichtenfelderi-huuliensis | –0.06878479 | –0.094475902 | –0.043093678 | 4.25E-10 |
luii-huuliensis | –0.101777804 | –0.131262479 | –0.072293128 | 3.37E-10 |
luii-lichtenfelderi | –0.032993014 | –0.057865404 | –0.008120623 | 0.00377334 |
forelimb length (FLL) | ||||
huuliensis-catbaensis | –0.137477526 | –0.199198043 | –0.075757008 | 9.51E-08 |
lichtenfelderi-catbaensis | –0.338691314 | –0.386903935 | –0.290478693 | 3.37E-10 |
luii-catbaensis | –0.365692271 | –0.425393393 | –0.305991149 | 3.37E-10 |
lichtenfelderi-huuliensis | –0.201213788 | –0.263738975 | –0.138688602 | 3.37E-10 |
luii-huuliensis | –0.228214745 | –0.299972435 | –0.156457055 | 3.37E-10 |
hindlimb length (HLL) | ||||
huuliensis-catbaensis | –0.137477526 | –0.199198043 | –0.075757008 | 9.51E-08 |
The PCA analysis using habitat preference as the dependent variable among the four species, showed that the karst-adapted and granite-stream-adapted species plot separately as before along taxonomic lines and that collectively, the former have significantly longer axilla-groin lengths (AG); longer, wider, and thicker heads (HL, HW, and CH); longer snouts (SL); longer limbs (FLL and HLL); wider interorbital distances (IO); larger eyes (ED) and larger ear openings (AD) (Fig.
A. Principal component analysis using karst habitat preference and granite stream habitat preference as the dependent variables for G. catbaensis, G. huuliensis, and G. luii of the luii group and G. lichtenfelderii of the lichtenfelderi group. B. Violin plots overlain with box plots showing the range, frequency, mean (white dot), and 50% quartile (black rectangle) of the size-adjusted morphometric characters. Asterisks denote characters bearing statistically significant mean differences between the karst and granite-stream-adapted species based on student t-tests. Upper photo from Vuu et al. (2008). Lower photo from Hai Ngoc Ngo.
Summary statistics and principal component analysis scores for the mensural characters for Goniurosaurus catbaensis, G. huuliensis, G. luii, and G. lichtenfelderii. Abbreviations are listed in the Materials and methods.
PC1 | PC2 | PC3 | PC4 | PC5 | PC6 | PC7 | PC8 | PC9 | PC10 | PC11 | PC12 | PC13 | PC14 | |
Standard deviation | 2.62151 | 1.36659 | 1.03962 | 0.92238 | 0.82762 | 0.77172 | 0.71922 | 0.62534 | 0.54279 | 0.51042 | 0.44460 | 0.42745 | 0.41145 | 0.18664 |
Proportion of variance | 0.49088 | 0.1334 | 0.0772 | 0.06077 | 0.04893 | 0.04254 | 0.03695 | 0.02793 | 0.02104 | 0.01861 | 0.01412 | 0.01305 | 0.01209 | 0.00249 |
Cumulative proportion | 0.49088 | 0.62428 | 0.70148 | 0.76225 | 0.81118 | 0.85371 | 0.89066 | 0.9186 | 0.93964 | 0.95825 | 0.97237 | 0.98542 | 0.99751 | 1 |
Eigenvalue | 6.87232 | 1.86758 | 1.08081 | 0.85079 | 0.68496 | 0.59554 | 0.51728 | 0.39105 | 0.29462 | 0.26053 | 0.19767 | 0.18272 | 0.16929 | 0.03483 |
AG | –0.24490 | –0.08424 | 0.09672 | 0.10058 | –0.56138 | 0.67337 | –0.35690 | 0.01987 | –0.04902 | 0.07718 | –0.08231 | 0.03497 | –0.02384 | 0.01371 |
BW | –0.04928 | –0.61441 | –0.07471 | 0.28744 | –0.08051 | –0.01832 | 0.20859 | –0.63240 | –0.03995 | –0.19837 | 0.15593 | –0.11090 | 0.06221 | 0.01347 |
BH | –0.04819 | –0.61109 | –0.04352 | 0.29637 | 0.08259 | –0.06845 | 0.04189 | 0.71074 | 0.07724 | 0.07219 | –0.03719 | –0.04417 | –0.03405 | 0.02105 |
ND | –0.18533 | –0.11312 | 0.64606 | 0.12685 | 0.26270 | –0.29150 | –0.55437 | –0.15934 | –0.06520 | 0.16090 | –0.04518 | 0.00367 | 0.01346 | –0.01680 |
HL | –0.34765 | 0.02673 | –0.05102 | –0.02271 | 0.00465 | –0.10546 | –0.03065 | 0.01183 | 0.02638 | –0.32873 | 0.17358 | 0.23473 | –0.81798 | 0.00137 |
HW | –0.33156 | –0.06751 | –0.07095 | –0.08475 | 0.05312 | –0.03718 | 0.30763 | –0.17678 | 0.01022 | 0.48788 | –0.67604 | –0.04173 | –0.21464 | 0.01521 |
CH | –0.22962 | –0.07645 | –0.23672 | –0.12992 | 0.73588 | 0.52586 | –0.13009 | –0.06367 | 0.04671 | 0.02514 | 0.139 | 0.0252 | 0.08193 | –0.0003 |
IO2 | –0.34276 | 0.00113 | –0.05114 | 0.03079 | –0.01618 | –0.12015 | 0.10256 | 0.06796 | –0.38288 | –0.23806 | –0.14615 | 0.67256 | 0.40575 | –0.08672 |
SE | –0.32091 | 0.01885 | –0.14557 | –0.08578 | –0.10147 | –0.18206 | –0.18393 | –0.02718 | 0.77823 | –0.28404 | –0.17039 | –0.03379 | 0.27124 | –0.00567 |
ED | –0.32467 | 0.19657 | 0.01794 | 0.11714 | 0.06087 | –0.00844 | 0.0395 | 0.12818 | –0.36952 | –0.45307 | –0.20533 | –0.65522 | 0.08037 | –0.01989 |
EE | –0.08674 | –0.33966 | 0.34954 | –0.81367 | –0.09736 | 0.04251 | 0.1902 | 0.08589 | –0.05072 | –0.11731 | 0.09913 | –0.09141 | 0.05499 | 0.02214 |
AD | –0.19445 | 0.23327 | 0.54515 | 0.30447 | 0.06568 | 0.23322 | 0.5704 | 0.05955 | 0.28325 | 0.01759 | 0.2077 | 0.05512 | 0.05956 | 0.0013 |
FLL | –0.35278 | 0.08503 | –0.16262 | –0.01768 | –0.10677 | –0.18636 | –0.00643 | 0.02061 | –0.09402 | 0.28874 | 0.3664 | –0.07982 | 0.12433 | 0.73937 |
HLL | –0.34892 | 0.04532 | –0.17931 | –0.04073 | –0.1368 | –0.17019 | 0.00654 | 0.02352 | –0.04871 | 0.36988 | 0.42336 | –0.16275 | 0.07515 | –0.666 |
Geckos in general are particularly well-adapted to karstic landscapes (see
The ML and BI analyses of
Goniurosaurus kadoorieorum of the luii group (represented by only 16S) is nested within G. luii in both the ML and BI analyses, rendering G. luii polyphyletic (Fig.
Wide-ranging more inclusive studies pertaining to ecosystems management are becoming commonplace in light of climate change and widespread habitat destruction. Such studies reconcile data from a broad range of disciplines in order to address issues that may bear on ecosystems management. Foundational to many of these studies is a basic understanding of species ecology and habitat preference—correlated here with ecomorphology (
Integrating the phylogenetic patterns of biodiversity and the morphological adaptations of habitat preference that, in part, underpin species radiations, can fundamentally contribute to conservation management programs (
Unfortunately, Goniurosaurus species are particularly attractive (Fig.
For supporting fieldwork and issuing relevant permits, we thank the authorities of the Cat Ba National Park (CBNP), Hai Phong City, Huu Lien Nature Reserve, Lang Son Province, Bai Tu Long National Park, Quang Ninh Province, Tay Yen Tu Nature Reserve, Bac Giang Province, Yen Tu Nature Reserve and the Management Department of Ha Long Bay, Quang Ninh Province. We are thankful to N. H. Nguyen, C. T. Pham, T.Q. Phan, H.M. Tran (IEBR, Hanoi), H.Q. Nguyen (VNMN, Ha Noi), H.T. Ngo (HUS, Hanoi) for assistance in the field and laboratory. We are grateful to T. Pagel and C. Landsberg (Cologne Zoo), S.V. Nguyen, T.Q. Nguyen (IEBR, Hanoi), L.V. Vu and T.T. Nguyen (VNMN, Hanoi) for their support of conservation–based biodiversity research in Vietnam. Field surveys were partially funded by Cologne Zoo, the Wildlife Conservation Society (“WCS”) John Thorbjarnarson Fellowship for Reptile Research Grant, the Mohamed bin Zayed Species Conservation fund (Project: 170515492) to H. N. Ngo, the Goniurosaurus yingdeensis Population Conservation Research of Guangdong Shimentai National Nature Reserve, China. Cologne Zoo is partner of the World Association of Zoos and Aquariums (WAZA): Conservation Project 07011, 07012 (Herpetodiversity Research, Amphibian and Reptilian Breeding and Rescue Stations). Researches of Hai Ngoc Ngo are funded by the German Academic Exchange Service (DAAD). We thank Dr. Hidetoshi Ota for his insight on the microhabitat preferences of the species of the Goniurosaurus kuroiwae species group.