Research Article |
Corresponding author: Armando H. Escobedo-Galván ( elchorvis@gmail.com ) Academic editor: Aaron Bauer
© 2021 Tonatiuh Ramírez-Reyes, Ilse K. Barraza-Soltero, Jose Rafael Nolasco-Luna, Oscar Flores-Villela, Armando H. Escobedo-Galván.
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:
Ramírez-Reyes T, Barraza-Soltero IK, Nolasco-Luna JR, Flores-Villela O, Escobedo-Galván AH (2021) A new species of leaf-toed gecko (Phyllodactylidae, Phyllodactylus) from María Cleofas Island, Nayarit, Mexico. ZooKeys 1024: 117-136. https://doi.org/10.3897/zookeys.1024.60473
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We describe a new species of leaf-toed gecko of the genus Phyllodactylus from María Cleofas Island, the smallest island of Tres Marías Archipelago, Nayarit, México. Genomic, phylogenomic, and morphological evidence support that the new species presents a unique combination of diagnostic characters. Morphologically, the new species has a high number of tubercles, head to tail (mean 47), longitudinal ventral scales (mean 61), and third labial–snout scales (mean 26). Gene flow tests revealed the genetic isolation of insular populations from mainland counterparts. In addition, we confirmed the non-monophyly of P. homolepidurus and P. nolascoensis, and we show that the taxon P. t. saxatilis is a complex; therefore, we propose taxonomic changes within the saxatilis clade. The discovery of this new insular endemic species highlights the urgency of continued exploration of the biological diversity of island faunas of Mexico.
Endemic gecko, genomics, insular species, morphological traits, Tres Marías Archipelago
The family Phyllodactylidae currently includes 10 genera and 148 species of geckos (
In the late nineteenth century,
Recently,
María Cleofas Island was well described by
We performed diurnal and nocturnal surveys in all available habitats to assess the herpetofauna of the María Cleofas Island from May 2017 to August 2018. The survey consisted of 2–3 researchers walking ad libitum through the different types of vegetation on the island, examining every microhabitat that could be potentially utilized by amphibians and reptiles (Fig.
We used the generated variant calling format file (VCF) of Ramírez-Reyes et al. (unpublished data), which contains the genetic variants (SNPs) corresponding to the saxatilis clade. This VCF file contains 13 genotypes and 14,271 binary SNPs (8.1% missing data). We analyzed this VCF file in R, mainly using three packages: vcfR (
We elaborated a species tree in SVDquartets (
We collected meristic character counts (n = 104) and morphometric measurements (n = 117) of specimens with an electric digital caliper (resolution 0.00005"/0.01 mm). We examined 117 specimens from four scientific collections: Colección Nacional de Anfibios y Reptiles at Instituto de Biología (CNAR-IBUNAM), Museo de Zoología de la Facultad de Ciencias at Universidad Nacional Autónoma de México (
All measurements and counts followed the protocol of
We conducted multivariate analyses for morphological characters using PCA and MANOVA to determine significant morphological differences among species within the saxatilis clade. A one-way ANOVA was performed to compare the mean SVL of all species analyzed, as well as the differentiated characters suggested by
We analyzed the stomach content from 36 individuals during fieldwork using stomach flushing (
The FST values supported a very high genetic differentiation among the populations studied (FST = 0.82 on average among all populations; Table
Nei’s distances and pairwise FST below and above the diagonal, respectively, among the studied populations calculated from the SNP matrix. The Maria Cleofas Island (MCI) lineage is shown in bold.
P. delcampi | P. nolascoensis | P. homolepidurus | P. partidus | P. t. saxatilis (MCI) | P. t. saxatilis (C) | P. t. saxatilis (VU) | P. t. saxatilis (M) | P. t. saxatilis (Q) | |
---|---|---|---|---|---|---|---|---|---|
P. delcampi | – | NC | NC | NC | 0.99 | 0.96 | 0.98 | 0.95 | NC |
P. nolascoensis | 0.18 | – | NC | NC | 0.95 | 0.71 | 0.93 | 0.66 | NC |
P. homolepidurus | 0.18 | 0.02 | – | NC | 0.93 | 0.79 | 0.92 | 0.36 | NC |
P. partidus | 0.19 | 0.02 | 0.01 | – | 0.96 | 0.8 | 0.95 | 0.48 | NC |
P. t. saxatilis (MCI) | 0.18 | 0.02 | 0.03 | 0.03 | – | 0.86 | 0.94 | 0.83 | 0.91 |
P. t. saxatilis (C) | 0.18 | 0.02 | 0.02 | 0.02 | 0.03 | – | 0.86 | 0.72 | 0.69 |
P. t. saxatilis (VU) | 0.19 | 0.03 | 0.04 | 0.03 | 0.03 | 0.03 | – | 0.85 | 0.9 |
P. t. saxatilis (M) | 0.18 | 0.02 | 0.01 | 0.01 | 0.03 | 0.02 | 0.03 | – | 0.43 |
P. t. saxatilis (Q) | 0.18 | 0.02 | 0.01 | 0.01 | 0.02 | 0.02 | 0.03 | 0.01 | – |
Neighbor-joining (NJ) tree based on Nei’s genetic distance for five populations of P. t. saxatilis (Maria Cleofas Island, Cosala, Villa Union, Quintero, and Mocuzari), two populations of P. homolepidurus (San Pedro Nolasco Island and Ortiz) and P. partidus (Partida Island) from Mexico (island and mainland populations).
The species tree developed in SVDquartets showed a high percentage of compatible quartets (87.5%) versus incompatible quartets (12.5%). The recovered species tree shows that the mainland populations of P. t. saxatilis (North and South) are rendered non-monophyletic by P. nolascoensis, P. homolepidurus, and P. partidus. This result is broadly consistent with previous studies, in which the non-monophyly of P. t. saxatilis was demonstrated (
The results of the meristic counts and morphological measurements are summarized in Tables
Mean and (standard deviation) of meristic characters examined for species studied. In bold we show the set of diagnostic meristic characters of P. cleofasensis sp. nov.
Species | L4AR | L4AL | L4PR | L4PL | THT | TAG | RTD | IS | SBI | TSS | SEN | SBP | SAV | SLV |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
P. cleofasensis sp. nov. | 11.71 (1.49) | 12.63 (0.51) | 13.25 (1.03) | 13.67 (1.22) | 47.89 (7.3) | 24.78 (4.86) | 15 (0.75) | 21.44 (2.40) | 7 (0) | 26.55 (2.35) | 12.55 (0.52) | 7.33 (0.5) | 27.22 (3.8) | 61 (4.33) |
Phyllodactylus sp. (Sonora) | 11.56 (1.04) | 11.6 (0.80) | 12.63 (1.09) | 12.70 (0.90) | 31.36 (4.51) | 20.48 (2.71) | 13.24 (1.25) | 21.96 (2.59) | 6.78 (0.69) | 24.30 (1.77) | 11.18 (0.95) | 7.48 (0.97) | 26.7 (3.48) | 58.03 (3.84) |
P. saxatilis | 10.87 (0.64) | 11.25 (1.03) | 12.25 (1.03) | 11.62 (0.74) | 32.32 (7.6) | 18.25 (3.99) | 13.62 (1.76) | 20.12 (2.53) | 6.5 (0.83) | 23.87 (1.95) | 11.75 (0.70) | 6.8 (0.64) | 26.37 (3.29) | 55 (3.96) |
P. nolascoensis | 10.5 (0.7) | 11 (1.41) | 12 (0.81) | 13 (1.15) | 41.75 (1.5) | 25 (3.55) | 15.25 (2.06) | 23 (3.26) | 7 (0) | 24.75 (1.5) | 12 (1.15) | 8 (0.81) | 24.75 (3.4) | 52.75 (1.89) |
P. magnus | 11.53 (1.14) | 11.75 (1.03) | 12.32 (1.14) | 11.95 (1.28) | 34.82 (5.80) | 21.90 (3.75) | 13.64 (1.47) | 22.46 (2.72) | 6.86 (0.53) | 25.59 (1.86) | 11.78 (0.90) | 6.73 (1.13) | 25.19 (2.13) | 55.30 (4.67) |
P. partidus | 10.8 (0.44) | 11 (0.70) | 11.8 (1.3) | 12 (0.81) | 33 (2.94) | 18.2 (3.11) | 13 (0.70) | 19.4 (2.07) | 6 (0.70) | 23.8 (2.38) | 11.6 (1.14) | 8.4 (0.54) | 27.2 (1.92) | 55.2 (2.77) |
Mean (and standard deviation) of morphometric characters (in millimeters) for the studied species.
Species | SVL | AG | HW | SE | ED | AO | IOD | IND | LFF | LFT |
---|---|---|---|---|---|---|---|---|---|---|
P. cleofasensis sp. nov. | 64.19 (10.38) | 25.42 (3.78) | 12.53 (2.45) | 9.37 (2.68) | 4.29 (0.45) | 2.53 (0.19) | 8.0 (1.61) | 2.12 (0.48) | 5.49 (0.98) | 6.37 (0.99) |
P. saxatilis | 65.44 (7.77) | 26.89 (2.61) | 12.23 (1.44) | 10.62 (1.14) | 3.97 (0.35) | 2.09 (0.37) | 8.20 (1.24) | 2.23 (0.33) | 4.82 (0.62) | 6.33 (1.08) |
Phyllodactylus sp. (Sonora) | 58.85 (7.36) | 23.01 (3.74) | 10.90 (1.45) | 9.25 (1.04) | 3.62 (0.45) | 1.82 (0.33) | 7.12 (0.89) | 1.83 (0.28) | 4.63 (0.77) | 5.76 (0.77) |
P. nolascoensis | 56.29 (2.54) | 23.85 (4.14) | 10.38 (0.35) | 8.95 (0.35) | 3.94 (0.16) | 2.17 (0.13) | 6.56 (0.13) | 1.9 (0.13) | 4.73 (0.35) | 5.15 (0.51) |
P. magnus | 73.03 (6.85) | 29.61 (3.33) | 13.51 (1.44) | 12.04 (1.14) | 4.68 (0.51) | 2.57 (0.47) | 8.85 (0.85) | 2.42 (0.36) | 5.72 (0.73) | 6.94 (0.92) |
P. partidus | 55.12 (4.89) | 20.71 (2.4) | 10.67 (1.29) | 9.19 (1.03) | 3.55 (0.46) | 1.97 (0.42) | 7.06 (0.85) | 2.08 (0.32) | 4.67 (0.50) | 5.49 (0.53) |
Summary of ANOVA tests for the morphometric character snout-vent length (SVL) and three meristic character: row dorsal tubercles (RDT), axilla-groin tubercles (AGT), and scales bordering postmentals (SBP).
Character | Df | Sum. Sq. | Mean sq. | F value | Pr (>F) |
---|---|---|---|---|---|
SVL | 5 | 5472 | 1094.4 | 20.38 | 2.38 × 10-14*** |
RDT | 5 | 34.35 | 6.87 | 3.71 | 0.00406** |
AGT | 5 | 324.4 | 64.87 | 5.326 | 0.000226*** |
SBP | 5 | 23.1 | 4.621 | 4.761 | 0.000616*** |
The PCA of morphometric data (excluding SVL) for the six species studied (Fig.
For the meristic characters, we performed the MANOVA excluding the SBI, TSS, and SEN characters since they did not show a normal distribution (or close to it). All MANOVA tests rejected the equality of multivariate means for all species analyzed (P < 0.001), Pillai trace (Trace = 1.51, d.f. = 5, F = 3.6, P = 1.73 × 10-14), Wilk's lambda (λ = 0.14, F = 3.9, P = 5.715 × 10-16), Hotteling test (HL = 2.66, F = 4.2, P = 2.2 × 10-16) and Roy test (R = 1.26, F = 10.5, P = 2.99 × 10-12). Once we determined that the multivariate means were not the same, we proceeded to perform individual ANOVA on paired comparisons of the most significant characters (P < 0.001), but emphasizing the differences of P. cleofasensis sp. nov. with respect to the others. For example, in the case of THT, P. cleofasensis sp. nov. differs significantly with respect to all species (P < 0.001) except P. nolascoensis, a pattern also seen with TAG and RTD characters. On the other hand, the ventral longitudinal scales demonstrated a significant difference between P. cleofasensis sp. nov. and P. magnus (P < 0.001), P. nolascoensis (P < 0.001), P. partidus (P = 0.009) and P. saxatilis (P = 0.002), while the lowest significance value for this character was with Phyllodactylus sp. (P = 0.04).
The present study constitutes a precedent for the taxonomy of the saxatilis clade (sensu Ramírez-Reyes et al. unpublished data) based on analyses of genomic and phylogenomic data. Here, our taxonomic treatment allows the use of specific categories for the studied populations and avoids non-monophyletic groups and infraspecific categories (P. t. saxatilis, P. homolepidurus). Specifically, in the case of the endemic population from the María Cleofas Island, the genomic evidence suggests that this population is clearly differentiated from its mainland counterparts (
Phyllodactylus tuberculosus
(in part) Wiegmann 1835 (
Phyllodactylus lanei
(in part)
P. tuberculosus saxatilis
(in part)
María Cleofas leaf-toed Gecko, Salamanquesa de la Isla María Cleofas.
Holotype: Adult female (MZFC-HE 35623) collected on María Cleofas Island (21.3095°N, 106.2340°W, WGS84, 64 m elev.) on 24–25 May 2018 by Ilse K. Barraza Soltero and Armando H. Escobedo Galván. Paratypes. All collected from the type locality, María Cleofas Island (Six adult specimens and two juveniles). MZFC-HE 35618-35622 and MZFC-HE 35624-35626.
Phyllodactylus cleofasensis is a species of medium to large body size. Snout-vent length of P. cleofasensis measured during fieldwork ranged from 44.8 to 77.0 mm (mean 59.5 mm). Concerning body size, P. cleofasensis differs (in mean size) from P. magnus (73.03), P. nolascoensis (56.29), P. partidus (55.12) and P. saxatilis (65.44). Phyllodactylus cleofasensis has a white venter, variable dorsal coloration, and a greater number of paravertebral dorsal tubercles (mean 47.89). Three meristic characters mainly differentiate P. cleofasensis from the rest of the species of the saxatilis clade (P. saxatilis, P. nolascoensis, P. partidus, P. homolepidurus and Phyllodactylus sp.) (Table
Adult female with SVL 71.17 mm, robust body, head not flattened, neck slightly differentiated from head. Head width 14.4 mm and snout length 12.11 mm. Rostral scale is flat (no grooves or stretch marks) and in contact with the two internasal scales. Nostril in contact mostly with the rostral scale and marginally with the first labial scale on both sides; supranasal scales in contact with 12 scales crossing from right to left side; 22 interorbital scales counted from middle of eye, interorbital distance 9.75 mm. 24 scales crossing snout between contralateral second labial scales 27 between third labial scales. Number of loreal scales 14 on right side and 15 on left side; equal number of supralabial scales (14), labial scales (8), and infralabial scales (7) on each side. Auricular opening oval (2.48 mm) smaller than the ocular opening, occipital scales similar in size and shape to interorbitals (not greatly differentiated in size and shape). Mental scale slightly wider than long, forming a “V” but not with pronounced angles; eight postmental scales in contact with first infralabials on both sides (right and left). Body with granular and circular scales interspersed with tubercles of different sizes; the specimen presents a fragmented tail. Internarinal distance 2.67 mm and axilla-groin length 26.19 mm. 14 rows of dorsal tubercles, 20 axilla-groin tubercles on right side and 19 on left side. Presents 29 transversal ventral scales with first ventral scale differentiated from lateral scales (which are small and circular). Ventral scales differentiated in size and shape from lateral and gular scales. Scales imbricate on extremities (anterior and posterior), as well as on dorsal region of the tail. No femoral or precloacal pores. Digital lamella formulae: right posterior (9-11-15-14-13), left posterior (8-10-11-12-13), right anterior (8-11-12-13-10), left anterior (8-10-12-13-11); fourth finger of extremities longer that others (5.55 mm manus, 7.49 mm pes); digital toepads longer than wide on all fingers.
Specific epithet is taken from the type locality María Cleofas Island, with the Latin suffix -ensis meaning, “originating from.” Specific epithet is masculine, in agreement with the gender of Phyllodactylus.
All meristic and morphometric characters are presented with mean values and standard deviation in Tables
Individuals of P. cleofasensis were observed active during night surveys under single rocks, abandoned anthropogenic structures, or in some cases on the trunk of Piranhea mexicana. Some were observed on the ground while they moved between rocks. In some parts of the island, they can be seen in abandoned man-made structures, which are shelters for species such as geckos, anoles, iguanids, and bats. Although predation of P. cleofasensis has not been reported, we suggest that Oxybelis microphthalmus (for taxonomic status see
Prey items identified from stomach contents of P. cleofasensis A Pycnoselus surinamensis B crickets of the family Rhaphidophoridae C beetles of the genus Telabis D Centruroides elegans insularis E Euphoria germinata F and G beetles of the family Elateridae H spider of the family Caponiidae I some individuals of lepidopterans.
Herein we present genomic, phylogenomic, and morphological evidence that demonstrates the independent species status of the endemic population of Phyllodactylus from María Cleofas Island. To our knowledge, the only work that mentioned morphological differences between the insular and mainland populations of P. t. saxatilis was conducted by
The phylogenetic position of P. cleofasensis was unknown until recently. Based on a relaxed molecular clock model, this species diverged from mainland populations during the late Miocene (~7 mya), and shows the highest genetic isolation of the species in the saxatilis clade (Ramírez-Reyes et al. unpublished data). The recovered species tree allows us to propose a more stable taxonomy for this clade, with a clear separation of P. homolepidurus and P. nolascoensis (as was recently proposed by
The three insular endemic species from Nayarit are differentiated morphologically. Phyllodactylus lupitae (SVL = 64.25) is the largest (mean body size), though very similar in size to P. cleofasensis (SVL = 64.19). The smallest species is P. isabelae (SVL = 45.91). Phyllodactylus lupitae is differentiated from P. cleofasensis by a smaller number of dorsal paravertebral tubercles (mean 28.82 versus 47.89). With respect to the continental species compared, we demonstrate that a set of diagnostic characters (THT, TSS, and SLV) allows a clear morphological differentiation of P. cleofasensis from the other Phyllodactylus species in Mexico (see Table
The stomach contents of P. cleofasensis coincide with those reported in other studies on Phyllodactylus species. We found coleopterans, arachnids, and orthopterans, as well as unidentifiable matter (vegetation, rocks, and insect wings) and shed skin remains.
Finally, a striking result was that we did not find non-native species during explorations on the island, despite María Cleofas Island having suffered ecological disturbances due to anthropogenic activities and the vestiges of man-made constructions visible. To our knowledge, non-native species have been reported on some islands pertaining to Nayarit, specifically the Common gecko Hemidactylus frenatus on María Madre Island (
The first author thanks the Posgrado en Ciencias Biologicas and Facultad de Ciencias, UNAM, for allowing him to complete his doctoral studies. The Consejo Nacional de Ciencia y Tecnología (CONACyT) awarded a doctoral scholarship to TR-R (CVU 586418) and a master scholarship to IKB-S (CVU 1065432). Fieldwork was supported by the Comisión Nacional de Seguridad (CNS), Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT), Secretaría de Marina (SEMAR), Complejo Penitenciario Federal Islas Marías, La Punta Outdoors S.A. de C.V., and Asociación Civil Protección y Restauración de Islas y Zonas Naturales (PROZONA AC). The staff of María Cleofas Research Boat provided logistical facilities to work on the island. Collecting permits SGPA/DGVS/01208/17 and SGPA/DGVS/010144/18 were issued by SEMARNAT. We appreciate the recommendations of Dr. Aaron Bauer (Villanova University) regarding nomenclature. We thank Ismael Huerta de la Barrera for her support in editing the map, figures, and photos. We thank Brett Butler for corrections and suggestions to the final English version. Finally, we thank the anonymous reviewers for their valuable comments and suggestions to improve this manuscript.