The evolution of hermit crabs (Crustacea, Decapoda, Anomura, Paguroidea) on the basis of carapace morphology: a state-of-the-art-report

ABSTRACT In our ongoing studies of both extinct and extant hermit crabs (Paguroidea Latreille, 1802), we have observed and recorded a number of morphological changes that have taken place between Early Jurassic times (c. 185 million years ago) and the present day. Species compositions of paguroid assemblages from marine Upper Jurassic and Lower Cretaceous rocks in Europe are here compared with those of modern marine settings. Basal paguroids with cylindrical carapaces predominated in reefal environments during the Late Jurassic, but were gradually replaced by hermit crabs with non-cylindrical carapaces. The most basal paguroids reveal a branchial groove, but branchial condensation towards a single (i.e., cervical) groove is here shown to have occurred early in their evolutionary history. In several extant, genera remnants of a branchial groove, in combination with several other basal features, can be seen. For this reason, these are here considered to be the most primitive members amongst extant paguroids. In this study, we resurrect the family Probeebeidae and erect a new family, Paguropsidae n. fam, to accommodate extant basal hermit crabs such as Paguropsis Henderson, 1888, Eopaguropsis Fraaije, Krzemiński, Van Bakel, Krzemińska & Jagt, 2012 and Paguropsina Lemaitre, Rahayu & Komai, 2018. Described are also one pair of Early Jurassic (Pliensbachian) and two pairs of Middle Jurassic (Callovian) isochelous paguroid chelae, all collected recently. A new specimen of Schobertella reveals some important morphological traits of the shield that had not been observed previously. The earliest known example to date of clearly heterochelous chelae in the fossil record of hermit crabs originates from upper Kimmeridgian/Tithonian strata in the Boulonnais (northwestern France). For the first time, a phylogenetic scheme of marine Paguroidea, as based on morphological data of carapaces, is presented.


INTRODUCTION
The classification of the superfamily Paguroidea Latreille, 1802, or hermit crabs, is by far the most convoluted amongst decapod crustaceans (McLaughlin et al. 2010) and fossil material has only rarely been considered in this respect. As a result of meticulous collecting from upper Mesozoic (Lower Jurassic-Upper Cretaceous) sedimentary rocks over the last twenty years, our insight into the diversity and evolutionary history of hermit crabs has greatly increased, despite the fact that details of paguroid evolution remain elusive. However, observations on morphological changes in (functional) hard parts can contribute in several ways to improving our understanding of evolutionary patterns and processes amongst paguroids. The identification of morphological novelties during the course of their Mesozoic evolution adds important data in unravelling their history.
In order to gain a better insight into evolutionary processes amongst paguroids, we here present an overview of all currently available palaeontological data with regard to faunal compositions and notable changes in the morphology of both carapaces and first pereiopods through geological time. Important basal morphological characters of carapaces observed in the fossil record are the following: 1. the presence of a branchial groove; 2. the presence of a long rostrum; 3. the possession of a well-ornamented carapace; 4. the presence of a mid-dorsal ridge on the shield; 5. the presence of a mesogastric process; 6. the possession of a well-calcified posterior carapace; 7. the presence of a calcified, delineated cardiac region. In view of the above, it is highly unfortunate that, to our knowledge, there is not a single study of extant paguroids in which details of carapace morphology are considered (Fraaije et al. 2019). As a consequence, there is quite a lot of confusion in the literature regarding the nomenclature of carapaces regions (and their delineation) in hermit crabs (see e.g., Morgan & Forest 1991). On the basis of new data from the fossil record and, in particular, of the notion of 'branchial condensation', described here, carapace delineation can be understood much more easily and used in interpretation of both extinct and extant paguroids effectively. It is our hope that the data presented here will stimulate biologists to start using carapace morphology in order to achieve a more robust phylogeny for the superfamily Paguroidea. Fraaije et al. (2012c) were the first to document an important trend seen in the carapace morphology of early (i.e., Late  Jurassic) paguroids. This concerns the fusion of the V-shaped branchial and subcircular cervical groove (as seen in, for instance, the genera Platykotta Chablais, Feldmann & Schweitzer, 2011, Eogastrodorus Van Bakel, Fraaije, Jagt & Artal, 2008and Gastrodorus von Meyer, 1864, into a single, sinuous groove (cervical groove) in Eopaguropsis Fraaije, Krzemiński, Van Bakel, Krzemińska & Jagt, 2012. This merger of two transverse carapace grooves into one, the cervical groove, is here referred to as 'branchial condensation' (Fig. 1); it occurs in all paguroid lineages. In some fossil and extant representatives, remnants of the branchial groove and/or small parts of the mesobranchial regions in between the cervical and branchial grooves can still be observed (see Figs 1B; 2). Traces of this double transverse groove system have been observed, amongst others, in the extant families Parapylochelidae Forest, 1987, Xylopaguridae Gašparič, Fraaije, Robin & De Angeli, 2016and Pylojacquesidae McLaughlin & Lemaitre, 2001.

BRANCHIAL CONDENSATION
Reduction in length of (spinose) RostRum One of the most basal paguroid genera known to date, Gastrodorus von Meyer, 1864, has a very long, spinose rostrum, with a midline crest that continues posteriorly towards the cervical groove. Amongst paguroid lineages in Mesozoic reefal settings, as inferred here, a rapid decrease in rostrum length has become apparent (Figs 2; 3).
Amongst extant paguroids only Probeebei Boone, 1926 (Boone 1926a), Tylaspis Henderson, 1885 and Paguropsis Henderson, 1888 have relatively long rostra with a midline crest. Apparently, a long spinose rostrum was advantageous only in certain deep-water habitats. Interestingly, but not unexpectedly, of the remaining extant groups, members of the basal family Annuntidiogenidae Fraaije, 2014 (which includes the genus Paguristes Dana, 1851) have relatively long rostra as well (Fig. 4C).
unifoRm caRapace oRnamentation When considering overall carapace morphology and, in particular, the presence of large, rimmed orbital cavities, the Triassic genus Platykotta may be interpreted as the most ancient paguroid known. This, as well as the Early Jurassic genera Schobertella Schweigert, Fraaije, Havlik & Nützel, 2013 and Eogastrodorus and the Late Jurassic to mid-Cretaceous Gastrodorus, all have uniformly granular to tuberculate shields and posterior carapaces (see e.g., Krzemińska et al. 2020

calcified and delineated caRdiac Region
Gastrodorids have a well-calcified and well-delineated cardiac region, while this region is in part well delineated in parapylochelids, probeebeids and paguropsids. Members of all other hermit crab families lack this character. tRends within paguRoid families Within the various families we have observed changes in a range of morphological features over geological time. For instance, in annuntidiogenids, a widening of the frontal shield has been observed in a number of species. In addition, the massetic region becomes bulkier and changes shape, from an elongated strip towards a more rectangular, globose part of the shield (Fig. 4).
Another trend is seen in the formation of, and a change in shape in, an intragastric Y-linea within the Calcinidae Fraaije, van Bakel & Jagt, 2017 (Fraaije et al. 2017(Fraaije et al. : fig. 2, 2020a. Unfortunately, the fossil record of paguroid carapaces of Paleogene and Neogene age is extremely scanty, with only a handful of specimens having been described to date. Needless to say, this hampers our understanding of paguroid age (Fraaije et al. 2012a: fig. 5a). The oldest members of the Paguridae known to date, of Tithonian age, also reveal a midline crest on the shield (Fraaije et al. 2019: figs 4a-c;5b).
In modern hermit crabs, only Probeebei, Tylaspis and Paguropsis show a midline crest on the rostrum that continues, to a greater or lesser extent, onto the shield.

mesogastRic anteRioR pRocess
In the Jurassic families Gastrodoridae, Schobertellidae, Diogenidae Ortmann, 1892, Paguropsidae n. fam (see below) and Parapylochelidae, a mesogastric anterior process is often present (see e.g., Fraaije et al. 2019: figs 2g-i;3a-e;4d). In modern paguroids, we have not been able to document any mesogastric anterior processes.   The first example of a hermit crab with a clear pair of heterochelous chelae (Fig. 7) is now contained in a private collection; it has been collected from the upper Kimmeridgian-lower Tithonian of the Atlantic Coast near Wimereux (Pas-de-Calais, northwest France). On the basis of a few photographs of this particular specimen that we have received from the collector, we have been able to document that the major right chela is about 1.5 to 2 times larger than the left one.
There is a match, in geological time, between this presence of heterochelous chelae in a Late Jurassic paguroid and the first occurrences of carapaces of members of the 'asymmetrically handed' Annuntidiogenidae, Diogenidae and Paguridae. Interestingly, the majority of extant primitive genera (e.g., The chelae of Schobertella simonsenetlangi were described in detail by Schweigert et al. (2013). They are convex both externally and internally and covered with about 20 irregular longitudinal rows of variably sized, forwardly directed tubercles on either side. The fixed fingers and dactyli are evolution during the Cenozoic (e.g., Beschin et al. 2016;Fraaije et al. 2020a;Wallaard et al. 2020). -Orhomalus spinosus Schweitzer, Feldmann & Lazăr, 2009, from the lower Callovian of Romania, and two newly collected specimens from the middle Callovian of France (Fig. 6). These individuals all reveal isochelous or near-isochelous chelae; they were collected during field work along the high-speed railway line LGV SEA (Ligne à Grande Vitesse Sud Europe Atlantique) by X. Valentin's team, from the Gratte-Loup limestones near Chasseneuil-du-Poitou (Vienne, France). These levels are dated as middle Callovian (Coronatum ammonite Zone; see Cariou 1980) and are situated near the historical quarries of Grand Pont, Bonnillet and Lourdines (Mathieu 1968). These specimens were associated with abundant bivalves, remains of marine crocodyliforms, plesiosaurs, sharks and bony fish, as well as terrestrial plants. These two pairs of chelae will be the subject of a forthcoming taxonomic study.

PAGUROID FAUNAL COMPOSITION THROUGH TIME
In order to document changes in paguroid faunal composition through time we have used three groups, namely the family Gastrodoridae, paguroids with 'cylindrical carapace' (i.e., all families depicted in Figure 12, to the left of the Gastrodoridae) and other ('non-cylindrical') hermit crabs (i.e., those to the right of the Gastrodoridae). The oldest known paguroid faunule based on carapace remains is that from the Oxfordian of southern Poland (Van Bakel et al. 2008;Fraaije et al. 2012bFraaije et al. , c, 2014aKrzemińska et al. 2016). This comprises a single species of gastrodorid, three pilgrimchelids, two pylochelids and a single paguropsid.
The Kimmeridgian assemblage from Nusplingen (southern Germany) has also been documented in detail in recent years (Fraaije 2014) and comprises at least two gastrodorids, three parapylochelids, two pilgrimchelids, three pylochelids, as well as one annuntidiogenid and one diogenid each.
So far, only a single mid-Cretaceous faunule is on record from the upper Albian of northwest Spain (Fraaije et al. 2008(Fraaije et al. , 2009(Fraaije et al. , 2012a, comprising one gastrodorid, one parapylochelid, one pylochelid and two annuntidiogenids. When percentages for these three groups are plotted (see Fig. 9), a significant decline in cylindrical paguroids, coupled with an increase in the numbers of non-cylindrical ones, can be noted. In modern reefal settings, there are no basal paguroids; instead, a predominance of asymmetrically handed paguroids is apparent. The most basal taxa amongst extant paguroids, such as parapylochelids, pylochelids, paguropsids and probeebeids, survived only in a few bathyal habitats and, in this way, are comparable to 'Lazarus' lobster taxa from such settings, such as Neoglyphea inopinata de Saint Laurent, 1975, Laurentaeglyphea neocaledonica Forest, 2006 andpolychelids (Polychelida).

ResuRRection of the family pRobeebeidae boone, 1926
The monotypic genus Probeebei, and its type species, P. mirabilis, were originally described as a primitive macruran by Boone (1926a). In the same year, Boone (1926b) erected a new family, the Probeebeidae, to accommodate this enigmatic crustacean. Much later, Wolff (1961) provided a detailed redescription of Probeebei and demonstrated that it was a hermit crab, which he assigned to the family Paguridae Latreille, 1802. The genus Probeebei was later transferred to the Parapaguridae Smith, 1882, by de Saint Laurent (1972). However, that author barely considered the carapace morphology of this genus, yet based her assignment to the Parapaguridae on features such as the presence of a labral spine, the absence of an exopodal flagellum on the first maxilliped, the presence of undivided abdominal tergites and an unpaired left gonopore in females and the lack of a median constriction on the telson (compare Lemaitre 1998). None of these characters was used in the descriptions of Probeebei and Tylaspis by de Saint Laurent (1972) and are not found either in any of the more recent accounts on parapagurid taxa (see e.g., Lemaitre 2013Lemaitre , 2014). An unpaired left gonopore is also a common trait in the Paguridae (e.g., Lemaitre 2003).
The monotypic genera Probeebei and Tylaspis were restudied and redescribed in detail by Lemaitre (1998), who noted that de Saint Laurent (1972) had erroneously indicated that she had examined specimens of Tylaspis anomala Henderson, 1885 from the Indian Ocean. In actual fact, this material had originated from the Pacific Ocean. Lemaitre (1998) also stated that several important morphological features of T. anomala had been inaccurately or insufficiently recorded in previous studies and found additional discrepancies or inaccuracies in published accounts of Probeebei and Tylaspis. He also observed a similar mode of life and identical morphological characters of the carapace (different from those of other parapagurids) for these two crab-like genera and assumed these two paguroids to be advanced forms. Our data show these two taxa retain almost all of the 'remnant' basal carapace characteristics mentioned above. For this reason, we consider them to be the most basal ones amongst extant paguroids. In fact, together with Parapylocheles Alcock, 1901, they are amongst the most primitivex of modern-day hermit crabs. diagnosis. -Shield (excluding rostrum) strongly convex, well calcified, width equal to length or width exceeding length, with distinct bulges (i.e., keraial and massetic regions) laterally, strong to weaker spinose ornament. Rostrum well developed, exceeding lateral projections. Cervical and branchial grooves subparallel, encompassing small branchial regions. Posterolateral margins spinose. Posterior carapace well calcified, broadly inflated, with dense spinose ornamentation. Well-developed cardiac grooves encompassing cardiac region.
RemaRks. -The bulges on the shield of extant probeebeids (Fig. 10) are quite similar to those of the most basal paguropsid, Eopaguropsis nidiaquilae (see Fraaije et al. 2012c: figs 2c;3), which also has a spinose ornamentation on the gastric and lateral parts of the shield.  Fraaije R. H. B. et al. of this genus amongst the Paguroidea, the taxonomy and morphology of Paguropsis typica have not been studied in any detail that would meet the requirements of modern paguroid studies (Lemaitre et al. 2018). Lemaitre et al. (2018) noted that Paguropsis was not monotypic any longer, and that in addition to P. typica, there was an additional genus and six species. The striking symmetry of the carapace, pereiopods (including chelipeds), uropods and telson, are unique amongst the so-called "asymmetrically handed" paguroids. In illustrations provided by Lemaitre et al. (2018: figs 2a-d and 18d, in particular), important, yet hitherto unobserved and/or unrecorded paguroid carapace features are shown for Paguropsis and Paguropsina. These features are: deep slits along the postfrontal ridges centrally posterior to the orbital cavity and centrally directed incisions near the cervical groove between the posterior margin and branchial area in the central part of the narrow lateral carapace lobe. These features are also seen in an Eocene paguroid from Italy (Beschin et al. 2021 (Fig. 11).
etymology. -The name is derived from the type genus. encompassing small branchial regions (= lateral lobes) or forming broad, sinuous groove. Shield well calcified, subtriangular or subrectangular; dorsal surface slightly vaulted with incomplete midline crest; welldelineated massetic region covered with numerous setal pits; posterior carapace less calcified, delineated cardiac region; uropods and telson symmetrical. Chelipeds subequal, similar in armature and setation.

PHYLOGENY OF THE PAGUROIDEA BASED ON CARAPACE MORPHOLOGY
Based on the data presented above and the stratigraphical ranges of extinct paguroid taxa based on carapaces, a phylogeny of all marine paguroids is here proposed (Fig. 12).
Overall, it can be concluded that branchial condensation within the Paguroidea appeared early in the Jurassic; it has also been recognised (and used for taxonomic purposes) in a wide array of Mesozoic brachyurans (Van Bakel et al. comm. pers.). Recognition and documentation of this phenomenon facilitate our understanding of paguroid carapace delineation. Together with other carapace characters, cheliped size and trends through time, as outlined above, the fossil data have contributed to the family tree of marine hermit crabs presented here. The occurrence of paired isochelous chelae and symmetrical calcified tergites in extinct paguroids (Fraaije et al. 2012d(Fraaije et al. , 2013c(Fraaije et al. , 2014b provides strong support for the symmetrical ancestry of the Paguroidea. Major Mesozoic evolutionary and radiation events amongst marine phyto-and zooplanktonic microbiota led, both directly and indirectly, to a rise of new ecological niches and, concomitantly, development of various marine benthic and nektonic groups (Fraaije et al. 2018). Linked to the occupation of these novel niches through time, shifts in carapace and cheliped morphologies occurred. A better-adapted metabolism and changes of food source also had an impact on gill structure and internal musculature and consequently led to internal rearrangement (e.g. Van Bakel et al. 2012). Additional material and more in-depth studies are needed to document the increased diversity in morphology, physiology and behaviour within the Paguroidea during deep time.

Acknowledgements
Our late colleague Patsy McLaughlin opened our eyes when, around 2007, we embarked on our studies of extinct hermit crabs, by hinting at the close relationships of our Late Jurassic material with the genera Paguropsis and Tylaspis and members of the family Pylochelidae; her assistance was instrumental in producing our 2008 paper. Dr Charles Fransen (Naturalis Biodiversity Center, Leiden, the Netherlands) supplied several items of literature for which we are grateful. G. G. and X. V. are appreciative to the municipality of Chasseneuil-du-Poitou (Mr C. Eidelstein) and to Mrs E. Blandin, P. Ferchaud and J. M. Terrasson for field assistance. Their work is supported in part by the Lisea Fondation Biodiversité (research grant 97 to Palaios association with the project "Past of Biodiversity from Vienne"). Hemke Dekkers, Shjalina Lentink, Mila van Loon, Lars Rongen, all students from SintLucas Vakschool voor creatief talent, Eindhoven, assisted in finishing all figures. Finally, comments made by Rok Gašparič (Kamnik/Ljubljana, Slovenia) and an anonymous reviewer on an earlier version of the typescript are much appreciated. Important synapomorphies include the following: 1, cylindrical carapace; 2, cervical and branchial grooves widely separated; 3, arrow-shaped gastric region; 4, cervical groove not extending to lateral border; 5, intragastric grooves; 6, Y-linea; 7, spinose posterolateral borders.