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Skeletal Variation in Extant Species Enables Systematic Identification of New Zealand's Large, Subfossil Diplodactylids

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Skeletal Variation in Extant Species Enables Systematic Identification of New Zealand's Large, Subfossil Diplodactylids Scarsbrook et al. BMC Ecol Evo (2021) 21:67 BMC Ecology and Evolution https://doi.org/10.1186/s12862-021-01808-7 RESEARCH Open Access Skeletal variation in extant species enables systematic identifcation of New Zealand’s large, subfossil diplodactylids Lachie Scarsbrook1*, Emma Sherratt2, Rodney A. Hitchmough3 and Nicolas J. Rawlence1 Abstract New Zealand’s diplodactylid geckos exhibit high species-level diversity, largely independent of discernible osteologi- cal changes. Consequently, systematic afnities of isolated skeletal elements (fossils) are primarily determined by comparisons of size, particularly in the identifcation of Hoplodactylus duvaucelii, New Zealand’s largest extant gecko species. Here, three-dimensional geometric morphometrics of maxillae (a common fossilized element) was used to determine whether consistent shape and size diferences exist between genera, and if cryptic extinctions have occurred in subfossil ‘Hoplodactylus cf. duvaucelii’. Sampling included 13 diplodactylid species from fve genera, and 11 Holocene subfossil ‘H. cf. duvaucelii’ individuals. We found phylogenetic history was the most important predictor of maxilla morphology among extant diplodactylid genera. Size comparisons could only diferentiate Hoplodactylus from other genera, with the remaining genera exhibiting variable degrees of overlap. Six subfossils were positively identifed as H. duvaucelii, confrming their proposed Holocene distribution throughout New Zealand. Conversely, fve subfossils showed no clear afnities with any modern diplodactylid genera, implying either increased morphological diversity in mainland ‘H. cf. duvaucelii’ or the presence of at least one extinct, large, broad-toed diplodactylid species. Keywords: Diplodactylidae, Ecomorphology, Geometric morphometrics, Hoplodactylus duvaucelii, Taxonomy Background (e.g. coloration and scalation), with interspecifc skeletal New Zealand’s lizard fauna is characteristic of isolated variation rarely analysed. Early anatomical studies [12], archipelagos, exhibiting high species endemism, exten- however, noted osteological diferences between the two sive in situ radiations [1, 2] and insular gigantism [3]. then recognized genera: Hoplodactylus (‘brown geckos’) Despite this diversifcation, the New Zealand Diplodac- and Naultinus (‘green geckos’); focussing on the neotenic tylids (compared with the New Caledonian radiation) are condition of Naultinus and the ‘primitive’ osteology relatively conserved in form; exhibiting reduced morpho- of the New Zealand Diplodactylidae. Despite these in- logical divergence at a similar evolutionary depth [2, 4]. depth comparisons, re-examination of generic level skel- Formal taxonomic descriptions of New Zealand diplo- etal variation in the context of current nomenclature is dactylid species [5, 6], similar to those of Australian [7, 8] required, given considerable taxonomic fuidity over the and New Caledonian representatives [9–11], have been last 65 years [13–15]. based exclusively on external morphological characters For example, allozyme [15, 16] and mitochondrial DNA [17, 18] analyses recognized three species complexes within the genus Hoplodactylus, corresponding to two *Correspondence: [email protected] broad morphological groupings: narrow-toed (H. granu- 1 Otago Paleogenetics Laboratory, Department of Zoology, University latus and H. pacifcus) and broad-toed (H. maculatus) of Otago, Dunedin, New Zealand Full list of author information is available at the end of the article clades [19]. Further taxonomic revision [2] separated © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Scarsbrook et al. BMC Ecol Evo (2021) 21:67 Page 2 of 10 multiple Hoplodactylus species complexes into fve gen- now outdated taxonomy; [23]), particularly in the identi- era (Dactylocnemis, Mokopirirakau, Toropuku, Tuku- fcation of ‘H. cf. duvaucelii’, New Zealand’s largest extant tuku and Woodworthia), with Hoplodactylus reserved diplodactylid. for H. duvaucelii and the extinct giant H. delcourti [12]. Hoplodactylus duvaucelii (‘Duvaucel’s gecko’) is a large, Conversely, the monophyletic genus Naultinus has been nocturnal species, with a pseudoendemic (realized) dis- historically over-split, separated into North and South tribution on predator-free islands in the Cook Strait and Island genera (Naultinus and Heteropholis respectively; of the north-eastern coast of the North Island (Fig. 1A; [13]), with Heteropholis later synonymised with Naulti- [28]). Prior to Polynesian (~ 1280 AD; [29]) and Euro- nus [19]. pean (efectively the late 1700s) arrival, ‘H. cf. duvaucelii’ Descriptions of these revised genera were based exclu- was widely distributed throughout the North Island [25], sively on external morphology [2]; with osteological dif- and the northwest and eastern South Island (Fig. 1a; [23, ferences only recognized for the frontal [21, 22], which 30–33]), evidenced by the presence of large, isolated dip- has led to assertions of skeletal uniformity at the species- lodactylid remains in Holocene predator (laughing owl level [23, 24]. In comparison, the identifcation of inter- and falcon) middens. Subsequent range contractions specifc skeletal variation in cranial elements of New occurred as a result of the synergistic efects of competi- Zealand’s large eugongyline skinks has enabled both dif- tive exclusion, direct predation by introduced mammals, ferentiation from smaller congeners [25], and description and degradation of forest habitat [25, 34]. Tis extensive of the extinct ‘giant’ Oligosoma northlandi [26, 27] from distribution across multiple biogeographic regions [23, Holocene subfossil remains. Classifcation of isolated dip- 35], given pronounced regional endemism recognised lodactylid remains however, has been restricted to size (or proposed) in other New Zealand diplodactylid genera comparisons with extant representatives (in reference to [1, 2], combined with the extinction of other large lizards Fig. 1 a Assumed Holocene distribution (red fll) of Hoplodactylus duvaucelii, showing extant modern northern/southern populations (circles, crosses and triangles) and subfossil collection localities (stars). Numbers denote sampled Holocene subfossil collection localities (1–7), with letters corresponding to subfossil specimens (A-J): Little Lost World, Waitomo (1—A); Companionway Cave, Waitomo (2—K); Mataikona River, Wairarapa (3—I); Gouland Downs, Tasman (4—G); Takaka Hill, Tasman (5—H); Ardenest, North Canterbury (6 – B/C/D/E/F); Earthquakes, North Otago (7—J). b Surface models of a diplodactylid maxilla in lateral (top), dorsal (middle) and medial (bottom) views demonstrating placement of fxed landmarks (black circles) and equally spaced semilandmarks (white circles). Numbers and C-prefxed numbers correspond to anatomical landmark descriptions (Additional fle 1: Table S2.3) Scarsbrook et al. BMC Ecol Evo (2021) 21:67 Page 3 of 10 in New Zealand [26, 27] implies unrecognized diversity diplodactylid genera (Dactylocnemis, Hoplodactylus, may exist within ‘H. cf. duvaucelii’; perhaps detectable Mokopirirakau, Naultinus and Woodworthia), for com- through fne-scale osteological analysis. Geometric mor- parison with Holocene ‘H. cf. duvaucelii’ subfossils. Tree phometrics [36], a method of statistical shape analysis main research questions are tested: (a) can recognised that enables improved detection and visualisation of sub- diplodactylid genera be distinguished based on maxilla tle morphological diferences (compared with traditional shape; (b) is size a reliable method for generic-level iden- linear-based morphometrics [37, 38]), has been widely tifcation of isolated cranial elements; and (c) have cryp- applied in herpetofaunal studies; including the success- tic extinctions occurred in the Diplodactylidae (with a ful discrimination of closely-related species [39–41] and focus on ‘H. cf. duvaucelii’)? classifcation [42–44] of isolated cranial elements. We therefore predict osteological diferences, if examined Results appropriately (using geometric morphometrics), will be Principal axes of diplodactylid maxilla variation sufcient for discriminating between extant diplodactylid Principal component (PC) analysis of landmarked max- genera (and potentially species), enabling the identifca- illae (Fig. 1b) reveals the majority (71.5%) of shape vari- tion of isolated subfossil material, or reveal unidentifed ability among extant New Zealand diplodactylids is taxa that require description and diagnosis. concentrated in four dimensions
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