Research Article |
Corresponding author: Marshal Hedin ( mhedin@mail.sdsu.edu ) Academic editor: Gonzalo Giribet
© 2016 Angela DiDomenico, Marshal Hedin.
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:
DiDomenico A, Hedin M (2016) New species in the Sitalcina sura species group (Opiliones, Laniatores, Phalangodidae), with evidence for a biogeographic link between California desert canyons and Arizona sky islands. ZooKeys 586: 1-36. https://doi.org/10.3897/zookeys.586.7832
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The western United States is home to numerous narrowly endemic harvestman taxa (Arachnida, Opiliones), including members of the genus Sitalcina Banks, 1911. Sitalcina is comprised of three species groups, including the monospecific S. californica and S. lobata groups, and the S. sura group with eight described species. All species in the S. sura group have very small geographic distributions, with group members distributed like disjunct “beads on a string” from Monterey south to southern California and southeast to the sky-island mountain ranges of southern Arizona. Here, molecular phylogenetic and species delimitation analyses were conducted for all described species in the S. sura group, plus several newly discovered populations. Species trees were reconstructed using multispecies coalescent methods implemented in *BEAST, and species delimitation was accomplished using Bayes Factor Delimitation (BFD). Based on quantitative species delimitation results supported by consideration of morphological characters, two new species (Sitalcina oasiensis sp. n., Sitalcina ubicki sp. n.) are described. We also provide a description of the previously unknown male of S. borregoensis Briggs, 1968. Molecular phylogenetic evidence strongly supports distinctive desert versus coastal clades, with desert canyon taxa from southern California more closely related to Arizona taxa than to geographically proximate California coastal taxa. We hypothesize that southern ancestry and plate tectonics have played a role in the diversification history of this animal lineage, similar to sclerophyllous plant taxa of the Madro-Tertiary Geoflora. Molecular clock analyses for the S. sura group are generally consistent with these hypotheses. We also propose that additional Sitalcina species await discovery in the desert canyons of southern California and northern Baja, and the mountains of northwestern mainland Mexico.
Species delimitation, plate tectonics, short-range endemism, historical biogeography, Bayes Factor Delimitation, Madro-Tertiary Geoflora
Laniatorean harvestmen comprise the majority of Opiliones diversity, with more than 4100 described species (
The phalangodid genus Sitalcina is comprised of three species groups (
Habitats and live in situ specimens. A Granite talus at Mt Palm Springs, CA – creosote + ocotillo + bursage habitat B live S. borregoensis from Mt Palm Springs C Volcanic talus at Peeples Valley, AZ – pinyon, juniper habitat D live S. rothi from Peeples Valley E live S. peacheyi from Madera Canyon, AZ F live S. sura from Palo Colorado Road, CA. Specimen images not at same scale.
Because of apparent limited dispersal abilities and microhabitat specificity, extreme population genetic structuring and divergence can be expected in Sitalcina, as is observed in other low vagility Laniatores (e.g.,
A variety of objective species delimitation methods have been developed in recent years (e.g.,
In this research we first use species discovery approaches to formulate alternative species delimitation hypotheses for the S. sura group. Based on genetic species delimitation results, supported by consideration of morphology, two new species and the previously unknown male of S. borregoensis are described. A time-calibrated multilocus species tree is used as a framework to interpret the biogeographic history of the S. sura group. We hypothesize that this history is linked to both plate tectonics and southern ancestry, similar to elements of the MTG.
Fieldwork was conducted in the winter and spring months when surface microhabitats were most suitable for successful collections. Voucher specimens used for morphological study and species descriptions were preserved in 80% ETOH, while those used in genetic analyses were preserved in 100% ETOH at -80 °C. All described species of the S. sura group were collected from at or near type localities (
Genomic DNA was extracted from leg tissue (2–3 legs) using the Qiagen DNeasy Kit (Qiagen, Valencia, CA). DNA fragments for mitochondrial cytochrome oxidase I (COI) and nuclear 28S rRNA, plus five additional protein-coding nuclear genes, were amplified using PCR (Table
Gene name, matrix completeness, aligned length, parsimony informative sites (ingroup), evolutionary and clock models.
Gene name | Ixodes homolog | Matrix % Complete | Aligned length | PI sites | Model of evolution | Clock model |
---|---|---|---|---|---|---|
Ecotropic viral integration site protein, putative | ISCW 021220 | 75% | 508 bp | 58 | HKY+I | Relaxed |
Protein phosphatase 2A regulatory subunit A, putative | ISCW 003443 | >75% | 242 bp | 37 | HKY+ Γ | Strict |
RING finger protein, putative | ISCW 003817 | >95% | 214 bp | 32 | GTR+I | Strict |
Protein transport protein Sec24A, putative | ISCW 016134 | >95% | 364 bp | 37 | GTR+ Γ | Relaxed |
Neuromusculin, putative | ISCW 006547 | >95% | 197 bp | 22 | HKY+ Γ | Relaxed |
28S | >95% | 1094 bp | 71 | GTR+I+ Γ | Relaxed | |
COI (all) | 100% | 549 bp | 249 | GTR+ Γ | Relaxed | |
COI (pos1) | GTR+ Γ | |||||
COI (pos2) | HKY+I+ Γ | |||||
COI (pos 3) | GTR+Γ |
Models of DNA sequence evolution were chosen using jModeltest2 (
We used genetic clustering in the initial “discovery” phase of species delimitation, a procedure common in the recent literature (reviewed in
Multilocus species trees were reconstructed using *BEAST 1.8 (
Divergence time analyses were performed in *BEAST (
Bayes factor delimitation (BFD,
Hypothesis | Distinct Species (total in parentheses) | Motivation |
---|---|---|
H1 | Glen Oaks, Santa Ynez, S. borregoensis, Borrego Palm Canyon, S. catalina, S. chalona, S. flava Topanga, S. flava Piuma + Palos Verdes, S. peacheyi, S. peacheyi MAD, S. rothi, S. sura, S. seca (13 species) | Following STRUCTURE admixture model |
H2 | Glen Oaks, Santa Ynez, S. borregoensis, Borrego Palm Canyon, S. catalina, S. chalona, S. flava Topanga, S. flava Piuma + Palos Verdes, S. peacheyi, S. peacheyi MAD, S. rothi, S. sura + S. seca (12 species) | Adjacent S. sura + S. seca considered a single species |
H3 | Glen Oaks, Santa Ynez, S. borregoensis + Borrego Palm Canyon, S. catalina, S. chalona, S. flava Topanga, S. flava Piuma + Palos Verdes, S. peacheyi, S. peacheyi MAD, S. rothi, S. sura, S. seca (12 species) | Anza-Borrego specimens considered a single species |
H4 | Glen Oaks, Santa Ynez, S. borregoensis, Borrego Palm Canyon, S. catalina, S. chalona, S. flava Topanga, S. flava Piuma + Palos Verdes, S. peacheyi + S. peacheyi MAD, S. rothi, S. sura, S. seca (12 species) | S. peacheyi as single species |
H5 | Santa Ynez, S. borregoensis, Borrego Palm Canyon, S. catalina, S. chalona, S. flava Topanga, S. flava Piuma + Palos Verdes, S. peacheyi, S. peacheyi MAD, Glen Oaks + S. rothi, S. sura, S. seca (12 species) | Coastal STRUCTURE results + Desert no-admixture model results |
H6 | Glen Oaks, Santa Ynez, S. borregoensis, Borrego Palm Canyon, S. catalina, S. chalona, Palos Verdes + S. flava, S. peacheyi, S. peacheyi MAD, S. rothi, S. sura, S. seca (12 species) | S. flava and Palos Verdes as single species |
H7 | Glen Oaks, S. borregoensis, Borrego Palm Canyon, S. catalina, S. chalona, Santa Ynez + S. flava + Palos Verdes, S. peacheyi, S. peacheyi MAD, S. rothi, S. sura, S. seca (11 species) | coastal southern CA a single species |
H8 | Glen Oaks, Santa Ynez, S. borregoensis + Borrego Palm Canyon, S. catalina, S. chalona, S. flava Topanga, S. flava Piuma + Palos Verdes, S. peacheyi + S. peacheyi MAD, S. rothi, S. sura, S. seca (11 species) | S. peacheyi as single species; Anza-Borrego specimens considered a single species |
H9 | S. borregoensis + Borrego Palm Canyon, S. catalina, S. chalona, S. flava +Santa Ynez + Palos Verdes, S. peacheyi + S. peacheyi MAD, S. rothi + Glen Oaks, S. sura + S. seca (7 species) | Putative species grouped with geographic neighbors |
With incomplete knowledge of the full distribution of the S. sura group, possible regions with additional new populations or species were identified via ecological niche modeling (ENM). DIVA-GIS (
Male penises that were not protruding from the genital operculum were physically extracted using a blunt insect micro pin. Exposed penises were placed in room temperature (or hot) 10% KOH for 1-2 minutes for expansion. Female ovipositors were exposed using the same blunt pin procedure. Specimens were imaged using a Quanta 450 scanning electron microscope (SEM) after being mounted and coated with 20nm platinum. One or two specimens were used for SEM as needed. Whole specimen digital images were captured using a Visionary Digital BK plus system (http://www.visionarydigital.com). Individual images were merged into a composite image using Helicon Focus 6.2.2 software (http://www.heliconsoft.com/heliconfocus.html). Specimen measurements were taken with an SZX12 Olympus dissecting scope equipped with an ocular micrometer, at 50× magnification.
DNA sequence data were collected for two outgroup taxa (data for S. lobata from transcriptomes), eight described species from the S. sura group, and four novel geographic populations with morphological features placing them in the S. sura group (see diagnostic features below). Not all specimens were successfully amplified for all gene regions, resulting in some missing data (Table
Mitochondrial COI gene trees were reconstructed using both a codon partitioned and un-partitioned model, and are generally topologically similar (Figure
Despite expected variance in nuclear gene tree topologies, several general trends are apparent. First, a coastal CA clade is recovered (generally with strong support, PP > 0.95) in all six nuclear gene trees (Figure
Nuclear gene trees. Individual genes include A Protein phosphatase 2A regulatory subunit A B Neuromusculin C Protein transport protein Sec24A D 28S, E RING finger protein, and F Ecotropic viral integration site protein. Outgroups trimmed from all trees except for 28S. Asterisks indicate posterior probabilities above 0.95. Desert taxa shaded.
STRUCTURE analyses for coastal clade specimens favor a K = 6 model (Figure
*BEAST analyses conducted with admixture STRUCTURE clusters as a priori species recover desert and coastal clades with strong support (PP > 0.95, Figure
*BEAST species trees. A Includes summary of STRUCTURE and BFD species delimitation results. Outgroup taxa not shown B Includes divergence time estimates based on
Using the
Model | Papadopoulou partitioned COI rate | Papadopoulou unpartitioned COI rate | Derkarabetian COI rate |
---|---|---|---|
tMRCAS. sura group | 18.25 (12.88–25.26) | 19.36 (13.58–26.47) | 29.43 (19.56–40.87) |
tMRCA coastal clade | 10.12 (6.88–14.03) | 10.98 (7.56–14.85) | 16.25 (10.57–23.07) |
tMRCA desert clade | 7.09 (4.85–10.01) | 7.49 (5.09–10.37) | 11.39 (7.64–16.04) |
tMRCAS. borregoensis, S. oasiensis | 4.86 (2–7.95) | 5.32 (2.09–8.57) | 7.87 (3–13.22) |
Precipitation in the coldest quarter (BIO19) and precipitation in the driest month (BIO14) were the best predictors of S. sura group distributions. ENMs based on these variables provide a visualization of possible sampling gaps within the S. sura group (Figure
BFD results support a 13 species model, following the K = 6 STRUCTURE model for coastal taxa and the K = 7 model for desert taxa (Tables
Model | Path Sampling | Bayes Factor PS | Stepping Stone | Bayes Factor SS |
---|---|---|---|---|
H1 | -12137 | NA | -11953 | NA |
H2 | -12387 | 499 | -12366 | 827 |
H3 | -12308 | 342 | -12252 | 598 |
H4 | -12258 | 241 | -12137 | 369 |
H5 | -12303 | 331 | -12235 | 563 |
H6 | -12235 | 196 | -12129 | 351 |
H7 | -12264 | 253 | -12140 | 373 |
H8 | -12352 | 429 | -12300 | 693 |
H9 | -12287 | 300 | -12131 | 357 |
Genetically distinct and morphologically diagnosable populations from Borrego Palm Canyon and Santa Ynez are formally described below. Also, previously unknown males of S. borregoensis are described. Following
Morphological abbreviations (following
Diagnosis. As presented in
Diagnosis. Members of the S. sura group are distinguished from related S. californica and S. lobata by the following characters (
Sitalcina borregoensis Briggs, 1968: 30.
Holotype female from California, San Diego County, Anza- Borrego Desert State Park, Mountain Palm Springs, collected by T. Briggs, April 5, 1967 (
This small-bodied species is most similar to S. rothi and S. oasiensis, with a low EM and a flattened body profile in both sexes. Females can be diagnosed by the moderately imbricate OVM. Males possess a TrIV spur that is approximately straight, and longer than in S. oasiensis. The distal end of PSL is conspicuously serrate.
FEMALE. As in
MALE. Integument color pale orange, appendages lighter. Body finely rugose with a few large tubercles on posterior tergites, one pair anteriorly on EM; 3 pairs of AT. EM low, flattened, eyes present. Palpal Fm with median dorsobasal row of 4 asetose tubercles and one small mesal tubercle. Palpal megaspines: trochanter one ventral and small; Fm 3 ventrobasal, one mesodistal; patella 2 mesal, one ectal; tibia and tarsus 2 mesal, 2 ectal. TC 3-5-5-5.
Measurements taken from following specimens: SDSU_OP3011 (SDSU_OP3010): BL 1.32 (1.24). SL 0.75 (0.84), SW 0.75 (0.78). EM width 0.19 (0.18), height 0.12 (0.10). GO length 0.17 (0.14), width 0.17 (0.14). Leg II length - missing (2.78), Leg II/SL - missing (3.31). TrIV spur present, nearly straight. Penis VP entire, apically pointed, with 8 pairs of setae, AS absent; glans DL quadrate; PSL serrate distally; S not visible.
New males were collected on 19 February, 2012 from the vicinity of the type locality. Suppl. material
Known only from the vicinity of Mountain Palm Springs, Anza Borrego Desert State Park. New collections are from a north-facing slope, under the first layer of granite rocks in a small ravine adjacent to a palm grove (Figure
Holotype male (SDSU_TAC000211, CASENT 9029998) from California, San Diego County, Anza-Borrego Desert State Park, Borrego Palm Canyon. N33.28025°, W116.43369° elev. ca. 430 m. Collected by A. DiDomenico, D. Carlson, S. Derkarabetian, S. Bejarano, February 23, 2013.
Named for the well-known palm oases of Borrego Palm Canyon.
Both sexes are small-bodied, with a low EM and a flattened body profile, similar to S. borregoensis. Females can be distinguished by the more strongly imbricate OVM. The male TrIV spur is approximately straight, shorter than in S. borregoensis.
Integument color pale orange with lighter appendages. Body finely rugose with larger tubercles along tergal margins and small tubercles anteriorly on EM; 2-3 pairs of AT. EM low and rounded, eyes present. Palpal Fm with median dorsobasal row of 3 asetose tubercles and one small mesal tubercle. Palpal megaspines: trochanter 2 ventral; Fm 3 ventrobasal, one mesodistal; patella 2 mesal, one ectal; tibia and tarsus 2 mesal, 2 ectal. TC 3-5-5-5.
MALE. Holotype (paratypes SDSU_TAC000297, SDSU_TAC000298): BL 1.3 (1.13–1.28). SL 0.81 (0.75- 0.8), SW 0.78 (0.73–0.88). EM width 0.19 (0.20), height 0.11 (0.10- 0.13). GO length 0.14, width 0.15. Leg II length 2.7 (2.34–2.64), Leg II/SL 3.33 (2.93–3.12). TrIV spur short, straight. Penis VP entire, apically rounded, with 9 pairs of setae, AS absent; glans DL quadrate; PSL simple and bilobed, rounded at apical end; S not visible.
FEMALE paratype SDSU_TAC000299: BL 1.5. SL 0.8, SW 0.9. EM width 0.25, height 0.13. Leg II length 3.0, Leg II/SL 3.75. Strongly imbricate OVM, apical teeth absent, 7 pairs of OVS, curved, multifurcate.
See Suppl. material
Known only from the type locality. Specimens were collected from sparse desert chaparral habitat, under small rocks amongst larger granite boulders, NE-facing slope above palm oases.
Holotype male (SDSU_TAC000216, CASENT 9029999) from California, Santa Barbara County, Santa Ynez Mtns, Montecito, E Mountain Drive, 0.4 mi NE from jct. with Cold Spring Road N34.45496°, W119.65288°, elev. ca. 230 m. Collected by A. DiDomenico, K. Emata, E. Garcia, A. Schönhofer, February 18, 2012.
This species is named in honor of Darrell Ubick (
Similar to other members of the northern coastal clade (S. sura, S. seca, S. chalona) in body form, relatively large-bodied, with a tall and pointed, tuberculate EM. Male TrIV spur curved, penis PSL similar to but distinguishable from S. chalona.
Integument color light orange with lighter appendages. Body finely rugose with larger tubercles along tergal margins and anteriorly on EM; 3-4 pairs of AT. EM tall, slightly pointed, eyes present. Palpal Fm with median dorsobasal row of 4 asetose tubercles and one small mesal tubercle. Palpal megaspines: trochanter 2 ventral; Fm 3 ventrobasal, one mesodistal; patella 2 mesal, one ectal; tibia and tarsus 2 mesal, 2 ectal. TC 3-5-5-5.
MALE. Holotype (paratypes SDSU_TAC000300, SDSU_TAC000301, SDSU_TAC000302): BL 2.1 (1.68–2.4). SL 1.14 (1.15–1.4), SW 1.3 (1.2–1.4). EM width 0.33 (0.35–0.4), height 0.23 (0.25–0.35). GO length 0.21, width 0.21. Leg II length 5.16 (4.2–5.12), Leg II/Scute Length 4.52 (3.14–3.66). TrIV spur short, curved. Penis VP entire, apically pointed, with 12 pairs of setae, AS absent; glans DL quadrate; PSL simple, rounded at apical end; S thick.
FEMALE. Paratypes SDSU_TAC000207 (SDSU_TAC000303, SDSU_TAC000304): BL 1.88 (1.7–2.0). SL 1.36 (1.0–1.25), SW 1.4 (1.25–1.35). EM width 0.36 (0.35), height 0.36 (0.2–0.25). Leg II length 4.48 (3.75–4.4), Leg II/Scute Length 3.29 (3.0–3.52). Slightly imbricate OVM, 6 pairs of OVS, straight, multifurcate.
See Suppl. material
Known only from the vicinity of Montecito, Santa Ynez Mountains, Santa Barbara County. Specimens were found under stones, in narrow ravine with stream, in a Quercus and Platanus forest.
This population was mentioned by
Species limits in the S. sura group were first studied by
Our results imply that some described species (e.g., S. peacheyi, S. flava) may actually comprise multiple cryptic species. This pattern is expected in a morphologically conservative group that occupies naturally fragmented habitats. This prediction would also apply to the geographically widespread S. californica (see
Sitalcina specimens are sometimes very challenging to collect. Specimens only occur near the surface (i.e., under accessible rocks or woody debris) at certain times of the year, apparently migrating deep into the soil matrix as surface conditions dry (
If multiple known species occur on the handful of sky-islands in southeastern Arizona, we expect additional undescribed species on the dozens of montane sky islands in northern Sonora. For many lineages, montane populations in southern Arizona constitute a “northern tip of a southern iceberg”, with centers of distribution found in northern Mexico (e.g., montane jumping spiders -
Niche modeling reveals a conspicuous geographic gap between habitats that are suitable for Sitalcina, separating eastern habitats in Arizona from western habitats in California (Figure
We failed to recover this predicted pattern, but instead recovered a well-supported phylogenetic pattern in both gene and species trees that includes the separation of S. sura group members into coastal versus desert clades (Figures
The fundamental spatial premise of our model is that the S. sura group has a center of origin in northwestern Mexico, perhaps centered around the region which is today the northern Gulf of California. The fundamental temporal premise is that initial diversification in the group happened before the Pacific plate began to migrate actively northwestwards (along the San Andreas Fault system) against a stationary North American plate (Figure
Our model has interesting connections to the botanical literature. As noted in the Introduction, most members of the S. sura group (and Sitalcina more generally) are found in habitats dominated by sclerophyllous woody plant taxa (e.g., Quercus, Pinyon pine, Arctostaphylos, Ceanothus, etc.). These plant lineages are part of a MTG, as originally defined by
Several predictions can be derived from our biogeographic model. First, we expect undescribed species in upland habitats of western Sonora, some of which may be related to California desert canyon taxa. Second, we predict undiscovered populations in desert canyons of northern Baja, and again predict possible mixed phylogenetic affinities (some coastal clade, some desert clade). Third, we predict that northern populations of S. californica on the North American plate (north of San Francisco) should be phylogenetically derived from southern populations on the Pacific plate (Figure
Both California and deserts of the American southwest are active areas for modern biogeographic research in animals. Despite this fact, we have found relatively few animal taxa that show biogeographic patterns similar to those observed in Sitalcina. Salamanders in the Batrachoseps pacificus group have a distribution much like the coastal clade (from Monterey south to northern Baja, almost all populations restricted to Pacific plate,
We have uncovered an apparently novel phylogenetic pattern in a biogeographically well-studied region. Our biogeographic model can be tested with additional research, both in Sitalcina, but also in other plant and animal lineages with similar geographic distributions.
We would like to thank Darrell Ubick and Thomas Briggs for their foundational work on Sitalcina, and expertise when needed for this project. We would also like to thank Dave Carlson, Alphonse DiDomenico, Kristen Emata, Erika Garcia, Casey Richart, Axel Schönhofer, Daniel Sitzmann, and Erik Stiner for their help with specimen collection. Sophia Bejarano, Alexa Feist, and Jeanne Rahe provided lab assistance, Joshua Coleman and Erik Ciaccio helped with image editing. Steve Barlow provided SEM support at SDSU. Shahan Derkarabetian helped to collect specimens, worked with ENM files, and edited the manuscript. Dean Leavitt clarified biogeographic patterns in Xantusia, and provided comments that greatly improved the manuscript. Ronald Clouse, Adriano Kury, Darrell Ubick and Gonzalo Giribet provided additional comments that improved the manuscript. Research was funded by grants to AD from the American Arachnological Society, Community Foundation Desert Research Grant, and the Anza-Borrego Foundation Howie Wier Memorial Conservation Grant, and an NSF grant awarded to MH (DEB 1354558).
Supplementary Tables 1–3
Table S1. Voucher and locality data
Table S2. PCR primer and reaction information
Table S3. GenBank accession information
Data type: Excel Table
Explanation note