Crocidura solita, Esselstyn & Achmadi & Handika & Swanson & Giarla & Rowe, 2021

Esselstyn, Jacob A., Achmadi, Anang S., Handika, Heru, Swanson, Mark T., Giarla, Thomas C. & Rowe, Kevin C., 2021, Fourteen New, Endemic Species Of Shrew (Genus Crocidura) From Sulawesi Reveal A Spectacular Island Radiation, Bulletin of the American Museum of Natural History 2021 (454), pp. 1-109 : 86-89

Crocidura solita , new species

LSID: urn:lsid:zoobank.org:act:B8B27A48-E1C7-47F1-B0B8-938722284C32

HOLOTYPE: MZB 43012 (= FMNH 213044 ), an adult male collected 1 March 2011 by J.A. Esselstyn. The specimen consists of a cleaned skull, fluid preserved body, and frozen tissue samples. External measurements from the holotype are 147 mm × 68 mm × 16 mm × 9 mm = 9.5 g. The voucher specimen with a tissue sample will be permanently curated at MZB, with an additional tissue sample retained at FMNH.

TYPE LOCALITY: Indonesia; Sulawesi Selatan; Enrekang ; Buntu Bato; Latimojong Village ; Karangan; Mt. Latimojong , Bantanase; 3.40755° S, 120.0078° E, 2050 m.

ETYMOLOGY: Solita is Latin for “usual,” used in recognition that this is another species of shrew with no striking phenotypic traits worthy of attaching a descriptive name.

GEOGRAPHIC DISTRIBUTION: We recorded Crocidura solita on three mountains in the west-central area of endemism (Mts. Latimojong and Rorekatimbo, Central Sulawesi Province; and Mt. Gandang Dewata, West Sulawesi Province; fig. 39 ). Records of this species span a broad range of elevations, from 700 to 2600 m. On Mt. Gandang Dewata, C. solita occurred syntopically with its sister species, C. ordinaria , at middle and high elevations (around 1600 and 2600 m; fig. 13 ; table 3 ).

DIAGNOSIS: A medium-sized shrew ( tables 2 , 14 ) with a medium gray dorsal pelage and lighter gray ventral pelage. Tail length is slightly shorter than head-and-body length ( fig. 9 ). The tail is only slightly bicolored, but some individuals have at least a few white applied hairs, giving it a somewhat silvery appearance, particularly near the tip. Dorsally, the feet are paler than the surrounding pelage, typically transitioning from light brown posteriorly to nearly white on the digits ( fig. 40C ). Ventrally, the feet are darker around the thenar and hypothenar pads than on the surrounding plantar and palmar surfaces; the hind feet tend to be darker than the forefeet. The external ears are slightly paler than the surrounding pelage. The mystacial vibrissae are short and mostly unpigmented, but a few of the longer, more posterior vibrissae are pigmented at their base. The skull is average in length (relative to HBL) for a Sulawesi shrew and slightly wide at the braincase and interorbital region relative to skull length ( fig. 10 ). The braincase is rounded, but with a somewhat prominent lambdoidal crest ( fig. 41C ). The suture between the squamosal and parietal bones is often open, leaving a long slit below the sinus canal. The interorbital region is well tapered. The maxillary bridge is thin.

COMPARISONS: For comparisons to most species, see the Crocidura ordinaria comparisons section above. Compared to C. ordinaria , the pelage is less dense (i.e., shorter hairs on the dorsum) and both the pelage and feet are paler on average and the body is less stocky ( fig. 17 ). The skull of C. solita is slightly smaller, and it is also narrower both absolutely and relative to skull length ( figs. 10 , 42 ), with a narrower palate and less robust dentition ( table 14 ). The suture between the squamosal and parietal bones is often open, leaving a long slit in C. solita , but this suture is usually closed in C. ordinaria .

COMMENTS: We posit that Crocidura solita and C. ordinaria are phenotypically similar sister species. Morphologically, we note subtle differences of body size, relative skull widths, and coloration. In the absence of other evidence, these slight morphological differences would be too little to justify dividing these specimens into two species, and we would not have suspected multiple taxa were represented by these specimens if it were not for our use of mitochondrial sequences. Syntopic specimens of these two species from Mt. Gandang Dewata are separated by a mitochondrial Jukes-Cantor distance of 0.064 (0.087 when all specimens are used in the calculation) and specimens of each species from the zone of parapatry is more closely related in the mitochondrial gene tree to conspecifics from other parts of the island ( figs. 4 , 5 ; supplementary data S2–S5). The mitochondrial distance between syntopic individuals and closer relatedness to allopatric populations suggests that these phenotypically similar animals are most likely evolving independently of each other.

In our mitochondrial gene trees, Crocidura ordinaria and C. solita are well-supported sister taxa and reciprocally monophyletic ( figs. 4 , 5 ). Our inferences using UCEs again indicate a close relationship with the two species forming a clade, but each species is reciprocally paraphyletic in our concatenated and species-tree inferences, the latter of which treated individuals as “species” and therefore did not force monophyly ( figs. 7 , 8 ). Our phylogenetic estimate from concatenated

nuclear exons also inferred reciprocal paraphyly for this species pair (supplementary data S6).

We tested species delimitation models with BPP between Crocidura solita and C. ordinaria using a dataset that included 64 C. solita and 22 C. ordinaria sampled from across their ranges. The alignment of five exons is 82% complete. All analyses of this dataset supported species delimitation with 1.0 posterior probability.

Overall, we interpret the combination of subtle morphological differences (weak evidence), deep mitochondrial divergence in the face of syntopy (strong evidence), and our BPP results (modest evidence) as supporting species distinction. We conclude that the paraphyly in our UCE inferences is most likely the result of incomplete lineage sorting and ancestral polymorphism. In coming to this conclusion, we are admittedly leaning heavily on mitochondrial data. However, the great differences between the mitochondrial sequences where the two species cooccur provides strong evidence for differentiation, at least between females. If these specimens represented a single species, we presume that any substantive gene flow would lead to one of the divergent mitochondrial types being favored, either because it is independently superior to the other, or because it is superior in its integrative functioning with the relevant parts of the nuclear genome (sensu Sloan et al., 2017; Hill, 2019). Mitochondria are foundational to energy metab- olism; viewing them as a neutrally evolving locus would ignore their functional importance and extensive interactions with nuclear gene products ( Nabholz et al., 2008; Lane, 2011; Sloan et al., 2017; Tobler et al., 2019). Although many cases of mitochondrial divergence within species have been documented, they rarely involve sympatry of the divergent mitochondrial types (but see Wayne et al., 1990; Morgan-Richards et al., 2017), and far more often than not, mitochondrial divergence is consistent with species limits ( Hebert et al., 2003; Monaghan et al., 2005; Esselstyn et al., 2012a; Cao et al., 2016). Taking in all the evidence, we believe these two sets of samples represent independently evolving populations that should be recognized as species despite the limited evidence for phenotypic or nDNA differentiation.

SPECIMENS EXAMINED: Mt. Gandang Dewata ( FMNH 218770 , 218773–218780 , 218976 ; MZB 34807 , 34811 , 34813 , 34814 , 34823 , 34826 , 34828 , 34829 , 34831 , 34881 , 34885 , 34887 ), Mt. Latimojong ( MZB 41669–41677 ; FMNH 213009 , 213012 , 213015–213019 , 213029 , 213031 , 213033–213037 , 213039–213043 , 213045– 213071 ; MVZ 237585–237593 , 237596 , 237598 , 237599 , 237611 , 237617 , 237619–237621 , 237628 , 237634 , 238122 ; MZB 43012 ; NMV C38479 , C38493 , C38516 ), Mt. Rorekatimbo ( FMNH 213163 , 213194–213245 , 213270 ), Rindingallo, Tana Toraja ( MSB 93125).

Figures

FIG. 39. Map of Sulawesi showing localities sampled for shrews. Colored areas enclose localities with known records of members of the Ordinary Group. To maintain clarity of presentation, the widespread Crocidura nigripes is not included.

FIG. 13. Elevational records of all species of Crocidura known from Sulawesi. Each point represents a specimen. For specimens associated with a minimum and maximum elevation, we used the center of the given elevational range. Sample sizes are given above the x-axis. Species are grouped according to the species groups used in the text (Thick = Thick-Tailed Group).

FIG. 9. Box plots showing variation in external measurements from all species of Sulawesi shrew. Plots show the median, 1st and 3rd quartiles, the maximum value within 1.5 × interquartile range (distance between 1st and 3rd quartiles; IQR), the minimum value within 1.5 × IQR, and outliers (black circles). Sample sizes are shown along the x-axis. Species are grouped according to the species groups used in the text (Thick = Thick- Tailed Group). All measurements in mm. HBL = head-and-body length.

FIG. 40. Images showing the ventral surface of the hind foot and dorsal surfaces of the tail base (approximately 1 cm from rump) and tail tip from three members of the Ordinary Group: A, Crocidura normalis, FMNH 213174 (left hind foot); B, C. ordinaria, FMNH 218726 (right hind foot); and C, C. solita, FMNH 213015 (left hind foot). Upper scale bar for foot, lower bar corresponds to both tail images.

FIG. 10. Box plots of relative skull measures showing braincase breadth (BB), interorbital width (IOW), and rostral length (RL) divided by condyloincisive length (CIL) and BB divided by IOW for all species of Sulawesi shrew. Plots show the median, 1st and 3rd quartiles, the maximum value within 1.5 × interquartile range (distance between 1st and 3rd quartiles; IQR), the minimum value within 1.5 × IQR, and outliers (black circles). Sample sizes are shown along the x-axis. Species are ordered according to the species groups used in the text (Thick = Thick-Tailed Group).

FIG. 41. Images showing dorsal, ventral, and lateral views of the skull and lateral and occlusal views of the dentary of three species belonging to the Ordinary Group: A, Crocidura normalis, FMNH 213457; B, C. ordinaria, FMNH 218726; and C, C. solita, FMNH 213044.

FIG. 17. Box plots showing the length of the hind foot (HF) relative to the head-and-body length (HBL) and the ratio of mass to HBL. Plots show the median, 1st and 3rd quartiles, the maximum value within 1.5 × interquartile range (distance between 1st and 3rd quartiles; IQR), the minimum value within 1.5 × IQR, and outliers (black circles). Sample sizes are shown along the x-axis. Species are ordered along the x-axis according to the species groups used in the text (Thick = Thick-Tailed Group). Lengths are in mm and mass is in grams.

FIG. 42. Box plots showing subtle differences in cranial measurements between Crocidura solita and C. ordinaria, two members of the Ordinary Group. Plots show the median, 1st and 3rd quartiles, the maximum value within 1.5 × interquartile range (distance between 1st and 3rd quartiles; IQR), the minimum value within 1.5 × IQR, and outliers (black circles). Sample sizes are shown along the x-axis. All measurements in mm.

FIG. 4. Maximum-likelihood estimate of the gene tree of Sulawesi Crocidura derived from an alignment of 851 individuals and 1111 characters from the mitochondrial gene cytochrome b. Bootstrap support is shown along branches. Clades corresponding to species are collapsed for ease of presentation. Tips are labeled with the species name, the number of tips (T), and number of localities (L), as labeled in figure 1, and the maximum intraspecific (MI) Jukes-Cantor distance calculated from a reduced alignment. Two species are paraphyletic and their respective, within-clade MI values are shown separately. For species described by Miller and Hollister (1921), the holotype or paratypes are included for C. elongata, C. lea, and C. rhoditis. Branch lengths between C. nigripes and other taxa are shortened for presentation. See supplementary data S2 for the full tree.

FIG. 5. Maximum likelihood estimate of the mitochondrial gene tree derived from an analysis of 14,007 characters (representing protein-coding and rRNA genes) from 83 samples. Bootstrap support values <95 are shown at nodes. Tips are labeled with the species, locality, and voucher number.

FIG. 7. Estimated species tree from analysis of 3940 ultraconserved element loci in ASTRAL. Samples from Sulawesi are labeled with the species name, locality, and catalog number. Asterisks indicate type specimens from Miller and Hollister (1921). Local posterior probabilities <0.95 are shown. Tip branch lengths are arbitrary.

FIG. 8. Estimated phylogenetic relationships from a maximum likelihood analysis of 983 concatenated ultraconserved elements. Samples from Sulawesi are labeled with the species name, locality, and catalog number. Asterisks indicate type specimens from Miller and Hollister (1921). Ultrafast bootstrap values <95 are shown.