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. 2022 Feb 25;17(2):e0264358. doi: 10.1371/journal.pone.0264358

Proteonematalycus wagneri Kethley reveals where the opisthosoma begins in acariform mites

Samuel J Bolton 1,*
Editor: Michael Scott Brewer2
PMCID: PMC8880937  PMID: 35213630

Abstract

It is generally thought that the anterior border of the opisthosoma of acariform mites is delineated by the disjugal furrow, but there is no evidence to support this other than the superficial appearance of tagmosis in some oribatids. It is proposed herein that the disjugal furrow is an apomorphic feature that does not correspond with any segmental borders. Although the disjugal furrow is absent from Proteonematalycus wagneri Kethley, the visible body segments of this species indicate that this furrow, when present, intersects the metapodosoma. Therefore, the disjugal furrow does not delineate the anterior border of the opisthosoma. Instead, this border is between segments D and E (segments VI and VII for all arachnids). This hypothesis can be accommodated by a new model in which the proterosoma warps upwards relative to the main body axis. This model, which is applicable to all Acariformes, if not all arachnids, explains the following phenomena: 1) the location of the gnathosomal neuromeres within the idiosoma; 2) the relatively posterior position of the paired eyes; 3) the shape of the synganglion; 4) the uneven distribution of legs in most species of acariform mites with elongate bodies.

Introduction

Mites comprise two superorders: Parasitiformes and Acariformes. Almost all mites have lost the furrows that delineate their body segments. However, the dorsal setae of acariform mites are arranged in transverse rows, which correspond with the underlying body segments [1]. There are conflicting interpretations concerning the homology of two of these segments, C and D (bearing setae c and d). Reuter [2] homologized segments C and D with the metapodosoma (segments V and VI for all arachnids [1]), which bears legs III and IV. More recently, the same interpretation was put forward by Weigmann [3] (Fig 1B). Van der Hammen [4] instead homologized segments C and D with the first two segments of the opisthosoma (segments VII and VIII) (Fig 1C and 1D), which was based on his hypothesis that the anterior border of the opisthosoma is represented by the disjugal furrow (Fig 1E). Many, if not most, acarologists accord with van der Hammen’s hypothesis by referring to the structures associated with segments C and D (principally setae and plates) as ‘opisthosomal’. The alternative term ‘hysterosomal’ (the region of the body that is behind the sejugal furrow), is neutral with respect to either hypothesis.

Fig 1. Terminology and models.

Fig 1

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A. Simplified representation of segmentation in mites, showing the segments in order but without any of the hypothesized modifications in shape. B. Interpretation of Weigmann [3]. C. Interpretation of Grandjean [5]. D. Interpretation of Klompen et al. [6] E. The three main body furrows of acariform mites. Roman numerals on the segments represent the segmental scheme commonly used for all arachnids [1]. Blue = proterosoma; yellow = metapodosoma; brown = opisthosoma; grey = neutral (no homologue applied); Pc = precheliceral region (acron); Ch = chelicera; Pa = palp; LI–LIV = legs I–IV; white arrowhead = abjugal furrow; black arrowhead = disjugal furrow; grey arrowhead = sejugal furrow.

Grandjean [5] based a widely cited model on van der Hammen’s hypothesis to explain the body segmentation of acariform mites. According to this model, the dorsal region of the podosoma (segments III–VI) is dramatically reduced, causing the parts of the body anterior and posterior to the podosoma to be pulled into areas that were occupied by the podosoma (Fig 1C). Klompen et al. [6] also adhered to van der Hammen’s hypothesis when they suggested an amendment to Grandjean’s model. They infer that the whole of the prosoma is somewhat evenly warped (Fig 1D), so that the dorsum of the podosoma is again represented as dramatically reduced. These interpretations are illustrated with an animation, which is accessible via the following link: https://zenodo.org/record/5512807#.YUOPiflKhaQ.

Perhaps the main reason that van der Hammen’s hypothesis has been so widely adopted is that it adds two additional segments to the acariform body (segments C and D are treated as separate from the metapodosoma), which makes the body segment count of this lineage closer to that of other arachnids [4]. However, this is not a strong argument because there is noticeable variation in the number of body segments among other arachnids; Scorpiones have nineteen body segments, whereas Opiliones have only fifteen [1].

Proteonematalycus wagneri Kethley, a rare species of mite that is only known from sandy habitats from the USA [7], is exceptionally useful for investigating the arrangement of body segments in Acariformes. Unlike other basal acariform mites, in which the furrows that delimit the segments are restricted to the dorsum (best exemplified by Terpnacaridae), some of the furrows of P. wagneri completely encircle the hysterosoma, clearly revealing which segments are associated with the metapodosoma. This mite was examined with a scanning electron microscope (SEM) and a light microscope.

Results

The integument of P. wagneri is extremely soft and fragile, causing it to readily distort when it is removed from alcohol. Alcohol stored specimens of this species completely shriveled up when viewed with cryo-SEM, which has been used with a high degree of success on other soft-bodied mites [8]. By comparison, specimens of P. wagneri that were desiccated using hexamethyldisilazane (HMDS) provided relatively good images under conventional SEM, although there was still some shriveling (Fig 2A and 2B). SEM reveals that each hysterosomal segment is clearly delimited by intersegmental furrows, which fall on either side of a transverse row of setae. A closeup of the integument shows that the striae break up into very fine protuberances along the base of each furrow (Fig 2B). By revealing furrows that correspond with the borders of all the hysterosomal segments, SEM removes any remaining ambiguity concerning the homology of the furrows with segmental borders. It should be noted that the drawings in the original species description do not include the furrow between segments F and H [7]. Despite the relatively low image resolution compared to that of SEM, light microscopy demonstrates how P. wagneri appears when it has not undergone any shriveling. This species reveals a series of very distinct intersegmental furrows (Fig 2C).

Fig 2. Proteonematalycus wagneri Kethley.

Fig 2

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A. Lateral view of female (SEM; FSCA 00030222). B. Lateral view of segments F–AN (SEM; same female as above). C. Lateral view of female, approximately 2 minutes after immersion in PVA (light microscopy; FSCA 00030224). Small white arrowheads point to the dorsolateral borders of coxae III and IV (note that there is slight sagging of the integument over the border of coxa III). White dotted lines delineate the borders of segments PS–AN.

Proteonematalycus wagneri shows that segments C and D bear legs III and IV, respectively, and so these segments represent the metapodosoma (Fig 2A). There is no trace of a disjugal furrow (see Discussion). Note that the borders that are highlighted with small white arrowheads (Fig 2A) represent the dorsolateral edges of coxae III and IV.

Discussion

Segmental homology

The presence of visible body segments, involving intersegmental furrows, is very clear in some soft-bodied basal acariform taxa [9, 10]. This is also the case in other basal arachnid lineages, for example, Mesothelae within Araneae [11, 12], and Opilioacarida within Parasitiformes [6, 13]. It is therefore appropriate to base the interpretation of acariform body segmentation on P. wagneri, which is a basal acariform mite with a complete set of intersegmental furrows along the hysterosoma.

The segmental homology of Acariformes has been problematical because almost all species show no visible trace of their underlying segments other than transverse rows of setae. Segments C–E (V–VII) bear the transverse rows of setae c–e, which can be readily homologized throughout Acariformes (with a number of exceptions due to hypertrichy). However, these transverse rows of setae are limited to the dorsum, and so it is almost always impossible to confidently determine the ventral extent of the borders of segments C–E. In some of the few acariform species where intersegmental furrows are exhibited, e.g., Terpnacaridae, those furrows do not extend to the venter of the hysterosoma.

But for segments C–E of P. wagneri, the entirety of each of the segmental borders are visible as furrows. Therefore, it is possible to use this very unusual feature of P. wagneri to determine the boundaries of segments C–E for Acariformes. P. wagneri reveals that segments C and D are metapodosomal (associated with legs III and IV), whereas segment E represents the first segment of the opisthosoma (Fig 2A). Mites in the family Tarsocheylidae also show this, although they have an incomplete set of intersegmental furrows along the hysterosoma [14]. These taxa affirm what has already been inferred from other taxonomic groups within Acariformes, namely Siteroptidae [2] and Oribatida [3].

The disjugal furrow

Van der Hammen [4] used the presence of the disjugal furrow in some oribatids to infer that the dorsum of the metapodosoma is dramatically reduced across all mites. However, there is no unambiguous evidence for the existence of a disjugal furrow outside of Oribatida. In Neognathus, longitudinal ridges of tubercles have been mislabeled as disjugal (each ridge cuts between setae c1 and c2 and so cannot delineate the anterior border of the C segment) [15]. And based on van der Hammen’s hypothesis, the term ‘disjugal’ is often applied to the dorsal part of the sejugal furrow of non-oribatid taxa [16–19].

The disjugal furrow runs from the front of segment C to behind legs IV. This furrow is absent in P. wagneri, but if it were present, it would have to cross over a vertical furrow that delineates the border between segments C and D (Fig 2A and 2C). Therefore, rather than form the boundary between the metapodosoma and prosoma, the disjugal furrow must intersect metapodosomal segments C and D (segments V and VI) (Fig 3A). And so, this furrow is an apomorphic feature that does not correspond with any segmental border. The disjugal furrow probably evolved as part of a suite of defensive modifications. Oribatids that have this feature are highly modified mites that have undergone a large degree of sclerotization compared to more basal lineages [20, 21]. It is relatively common for border-like structures to form in association with sclerotization. For example, labidostommatids have a distinctive groove that divides the body into a dorsal and ventral shield [22].

Fig 3. The metapodosoma of mites.

Fig 3

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A. Same model as Fig 1E, but color coded to show that the disjugal furrow intersects the metapodosoma (yellow). B. Opilioacarida, based on Klompen et al. [6]. Roman numerals on the metapodosomal segments represent the segmental scheme commonly used for all arachnids [1]. Blue = proterosoma; yellow = metapodosoma; brown = opisthosoma; black arrowhead = disjugal furrow. Thin black line delineates the border between segments C and D.

Clearly, the disjugal furrow is not evidence that all mites have a metapodosoma in which the dorsum is dramatically reduced relative to the venter. Indeed, no mites appear to have this modification. Proteonematalycus wagneri indicates that no such modification has occurred within Acariformes. In most of the main lineages of parasitiform mites the body segmentation is highly ambiguous. The single exception is Opilioacarida. Whereas the dorsum of the metapodosoma of this lineage was thought to be dramatically reduced [23], a more recent interpretation represents this reduction as relatively slight [6] (Fig 3B) (but note that Fig 6 of the same publication [6] appears to show no reduction at all).

A new model

Mites have been viewed as a distinctive lineage of arachnids based on the presence of a gnathosoma [24, 25], which represents an integrated mouthpart complex that articulates against the idiosoma (rest of the body). However, the gnathosoma is a pseudotagma because the associated neuromeres, the deutocerebrum and tritocerebrum, are located within the idiosoma [26]. Nonetheless, the body segments that are associated with the gnathosoma, segments I and II, are often represented as being anterior to the idiosoma [1, 3]. Accordingly, the neuromeres would have to have migrated, posteriorly, into the idiosoma [26]. But an alternative explanation for the relatively posterior position of the neuromeres is that the proterosoma warps upwards, relative to the main body axis, so that the gnathosoma is anterior to segments I and II (Fig 4A). These body segments, which contain the deutocerebrum and tritocerebrum, are part of the idiosoma rather than the gnathosoma. This would mean that the circumcapitular furrow, which delineates the boundary between the gnathosoma and idiosoma, would not correspond with any segmental border (except possibly the ventral part of the border between segments II and III). This is also a necessary implication of two of the other three main models [5, 6] (Fig 1C and 1D). Indeed, according to van der Hammen [27], the gnathosoma is a pseudotagma that is secondarily articulating, which implies that the circumcapitular furrow is not segmental in origin.

Fig 4. A new model.

Fig 4

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A. The proterosoma (anterolateral view). B. The body of an elongate bodied mite. Roman numerals on the metapodosomal segments represent the segmental scheme commonly used for all arachnids [1]. Blue = proterosoma; yellow = metapodosoma; brown = opisthosoma; PE = precheliceral region—epistomo-labral projection; PO = precheliceral region—ocular (also prodorsum or propeltidium); white dotted line delineates the circumcapitular furrow (boundary between gnathosoma and idiosoma).

Weigmann [3], Grandjean [5] and Klompen et al. [6] also proposed that the anterior region of the body is warped (Fig 1B–1D). According to Weigmann, only the gnathosoma is warped, but this fails to explain why the associated neuromeres are located within the idiosoma. This also does not explain the presence of eyes on the prodorsum or dorsal shield in many mites (see below). According to Grandjean and Klompen et al., the entire prosoma is warped. The metapodosoma is unwarped in the new model that is proposed herein (Fig 4B). This distinction is important because the region and extent of warping should have an effect on how body elongation proceeds in mites. If only the proterosoma is warped (in accordance with this new model), elongation of any of the proterosomal segments would extend the proterosoma along a vertical or oblique axis relative to the main axis of the body, causing the body to form a kink rather than become more elongated. But no such kink would arise to the body when the metapodosoma elongates because this part of the prosoma is aligned with the main axis of the body. Any dramatic elongation of the prosoma must therefore proceed via the metapodosoma rather than the proterosoma. This can explain the uneven distribution of legs in most species of acariform mites with elongate bodies (Fig 4B). Legs I and II are always tightly packed with the palps and chelicerae because the proterosoma does not elongate. But legs III and IV can shift to a much more posterior position because the metapodosoma is free to elongate [14, 28, 29] (Fig 2).

Warping of the entire prosoma or only of the gnathosoma cannot explain the uneven distribution of legs nearly as well. If the whole of the prosoma is warped, dramatic elongation should only occur to the part of the body that is posterior to legs IV, but this is clearly not the case. And if only the gnathosoma is warped, legs I and II should not always be tightly packed with the palps and chelicerae.

Upward warping of the proterosoma appears to be a feature of all arachnids. It would cause the part of the precheliceral region that bears the eyes to lie directly above the rest of the proterosoma, including the body segments that bear legs I and II. This can explain why various lineages, including Acariformes, Opilioacarida, Opiliones and Scorpiones, have eyes that are in a relatively posterior position on the prosoma, directly above the leg coxae. Moreover, the region of the synganglion that is associated with the proterosoma is also warped [30–33]. This part of the synganglion comprises the supraesophageal section and the first two neuromeres (associated with legs I and II) of the subesophageal section. The posterior part of the subesophageal section, which is associated with the metapodosoma, is more closely aligned with the main body axis. Therefore, the proterosomal warp may be a feature that is fundamental to the organization of the arachnid body. It is noteworthy that, primitively, the euarthropod is considered to have undergone tagmosis into a head (proterosoma) and trunk (hysterosoma) [34, 35]. Warping of the proterosoma may in some way be linked to this tagmosis.

A commonly held view of the prosoma of acariform mites is that the body segments that are associated with the gnathosoma, segments I and II, are anterior to the prodorsum, which would accordingly form the dorsum of segments III and IV [3, 36]. Consequently, the prodorsum would have no known homologue in other arachnids [1]. But if the proterosoma is warped, segments I and II cannot be anterior to the prodorsum. Instead, the prodorsum lies directly above these body segments (Fig 4A), which means that, sequentially, the prodorsum comes before them. Therefore, the prodorsum would be homologous with both the precheliceral region (excluding the labrum) and the propeltidium (the dorsal shield of the proterosoma), a structure that is found in Palpigradi, Solifugae and Schizomida.

In accordance with this new model, the proterosoma is warped and the metapodosoma is parallel, relative to the main body axis. There appears to be no arachnid that shows clear evidence that the metapodosoma is warped, whereas a warped proterosoma appears to be a feature of all arachnids. Therefore, this new model may be applicable to all arachnids.

Materials and methods

Collection

Proteonematalycus wagneri was collected from foredune sand using heptane flotation [37]. Collection event: U.S.A., Indiana, Porter Co., Indiana Dunes State Park, 41.6780 N 87.0081 W, sand dune (10 cm deep); collector: Samuel Bolton, 16 May, 2013 (FSCA 00030222: Female x1, Deutonymph x1, Protonymph x1, larva x1) (FSCA 00030224: Female x1; FSCA 00030225: Deutonymph x1).

SEM

Specimens of P. wagneri were transferred from a storage medium of 95% ethanol into the following series of solvents: 1) absolute ethanol; 2) 50:50 volume HMDS; 3) 100% HMDS. Immersion in each fluid medium lasted approximately five minutes. A minuten pin, which had been glued onto a FisherbrandTM plain wooden applicator, was used to maneuver the specimens between solutions. For the final step, the HMDS was left to evaporate. The specimens were then mounted on SEM stubs and sputter coated with approximately 70 nm of gold/palladium using a Denton IV sputtercoater. Micrographs were captured with a Phenom XL G2 Desktop SEM.

Light microscopy

Examination was with a compound microscope (Leica DM2500) equipped with differential interference contrast (DIC) and a digital SLR (Canon EOS 80D). Imaging was with a dry, 10x objective (brightfield). Polyvinyl alcohol (PVA) mounting medium was used to hold the specimens in a relatively still position. Specimens were imaged without a coverslip within minutes of being placed into the PVA. Contrast was heightened by setting the turret of the DIC between the 10 and 40 intervals.

Supporting information

S1 Fig. Larva FSCA 00030222.

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S2 Fig. Protonymph FSCA 00030222.

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S3 Fig. Protonymph FSCA 00030222.

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S4 Fig. Deutonymph FSCA 00030222.

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S5 Fig. Adult FSCA 00030222.

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S6 Fig. Deutonymph FSCA 00030225 (eight minutes after immersion in PVA).

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S7 Fig. Adult FSCA 00030224 (two minutes after immersion in PVA).

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Acknowledgments

Jonathan Bremer, at the Florida State Collection of Arthropods, undertook the SEM imaging of P. wagneri (Fig 2A and 2B). The U.S. National Park Service granted the author permission to collect from the Indiana Dunes National Lakeshore. The following individuals are thanked for their contribution through internal review and/or useful discussion: Erin Powell, Elijah Talamas, Paul Skelley (Florida Department of Agriculture and Consumer Services, Gainesville, Florida, USA) and Hans Klompen (Ohio State University, Columbus, Ohio, USA). The Florida Department of Agriculture and Consumer Services–Division of Plant Industry are thanked for their support on this contribution.

Data Availability

All relevant data are within the manuscript and its Supporting Information files. The minimal dataset is the images in Fig 2, which provides all the evidence needed for the discussion.

Funding Statement

The author received no specific funding for this work.

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Decision Letter 0

Michael Scott Brewer

5 Nov 2021

PONE-D-21-31633Proteonematalycus wagneri Kethley reveals where the opisthosoma begins in acariform mitesPLOS ONE

Dear Dr. Bolton,

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**********

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5. Review Comments to the Author

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Reviewer #1: Arachnids conventionally have a body divided into an anterior prosoma (or cephalothorax) and posterior opisthosoma (or abdomen), but in some groups the two body halves can fuse together to some extent which makes this fundamental division less obvious. The author has submitted an interesting manuscript which goes some way towards clarifying a long-standing problem of how to homologise the (reduced) body of acariform mites with those of other arachnids: in particular where does the opisthosoma begin? The author should be congratulated for producing high-quality images of a soft-cuticled species which I'm sure was challenging to handle, and makes a good case that the leg-bearing segments conventionally referred to as C & D belong to the metapodosoma part of the prosoma. The opisthsoma, in turn, begins behind the segment bearing the last pair of legs as in other arachnids. In this sense the study certainly merits publication and could be suitable for a journal such as PLOS One.

However, because its being submitted to a high-profile interdisciplianary journal (and not a specialist acarology publication) I think the manuscript could benefit from placing these results in a slightly broader context, making more comparisons with Arachnida in general. Essentially your data, as I understand it, suggests that the ground pattern of acariforms is a kind of straightforward 4+2 pattern of prosomal segmentation, immediately followed by the opisthosoma. This would make acariforms anatomically similar to things like schizomids, palpigrades and camel spiders (Solifugae). It may be worth noting that at least palpigrades and camel spiders have been proposed, in some phylogenies, as the putative sister-group of acariform mites.

As I'm sure the author knows there has also been a long history of mites being described using unique morphological terms, often with limited efforts to homologise them with structures in other arachnids. This hinders comparative morphology, and even phylogeny when homologous characters states are obscured by nomenclature. In the present case, would it be worth expressing the different hypotheses in terms of conventional numbering used in other arachnids? In other words, in the scenario of Weigmann and yourself C and D are prosomal segments 5 and 6, but in the other models they are opisthsomal segments 1 and 2 (or body segments 7 and 8). This could perhaps be done by adding segment numbers to Fig. 1A for example.

Related to this, I was thinking to what extent must we seperate dorsal elements from ventral (limb-bearing) elements. In lines 32 you say "There are conflicting interpretations concerning the relationship of these two segments, C and D...to the metapodosoma, which bears legs III and IV." I think what I'm getting at is which segments bear legs III and IV in the Van Der Hammen / Grandjean / Klompen scenarios? It can't be C and D, which they interpret as opisthosomal segments 1 and 2, so what, if anything, did they call the ventral metapodosomal elements bearing the last pair of limbs?

Another problem is that I couldn't wholly follow how you go from Figure 2A to Figure 3B, with the disjugal suture of oribatids cutting across one (or more) segments of the metapodosoma? You state that P. wagneri lacks a disjugal suture, which I'm sure from your photos is correct. I think the problem lies with lines 88-92 which should include a bit more detail about why the disjugal suture cannot be the typical arachnid prosoma/opisthosoma boundary, and what exactly you mean when you define a suture as something which only intersects a plane. How do you recognise this in actual specimens of mites? You propose that an intersegmental furrow is associated with a narrowing, but (to play devil's advocate) the disjugal suture in your idealised Fig. 3C could be seen as creating a slight fold or narrowing between the regions in front of and behind it. So why is it a suture (other than because of its traditional name?). In essence, your folded suture in Fig. 3B does not look like your smooth suture in Fig. 3A which, if anything, looks more like the prosoma-opisthosoma boundary in 3A.

Also, I did wonder if there is any embryological or hox gene work to support your model? Do the papers by Richard Thomas and/or Austen Barnett help? I recall that they found evidence for only 2 unequivocal segments in the oribatid opisthosoma, but did they indicate where (anatomically) the opisthosoma begins?

https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1525-142X.2012.00556.x

https://evodevojournal.biomedcentral.com/articles/10.1186/2041-9139-4-23

https://www.proquest.com/openview/f22b93c07a71a645657915c444208a67/1?pq-origsite=gscholar&cbl=18750

Again, the absence of segment numbers (or even the C, D, E scheme) makes it a little hard to follow the argumentation through into the higher oribatids and my question is, in the 3B model where (if anywhere) is the boundary between the segments bearing legs III and IV? The model implies it is not the disjugal suture, as this appears to originate behind leg IV, so have C and D (= 5 and 6) fused together here into an undifferentiated metapodosoma with (in your scenario) the disjugal suture arising as a novel structure and cutting across it?

The video of the body plan morphing into different hypotheses is nice. I'm not sure how much extra work is involved, but if they colour scheme used in Figure 1 were to be added it would be even clearer where different authors interpreted the start of the opisthosoma.

Other minor corrections

REFERENCES

May be a formatting problem, but genus and species names need to be italicised here throughout.

FIGURES

Figure 1: There is no part 'D' in the figure legend, but two part Es. I think it should read "D. Interpretation of Klompen et al. [6]"

Figure 2B: What is being highlighted by the white box? A furrow or protubrence? This is not really explained in the figure legend.

Reviewer #2: I am no expert in arthropod or mite segmentation, but this short paper appears to make a clear point about the need to adjust certain boundaries in body parts, namely the true border between opisthosoma and metapodosoma. The paper is straight to the point, clearly written and fairly strongly argued. The 2 main figures are extremely simple and clear (despite the complexity behind it), and the supplementary figs are also quite useful to support his hypothesis.

The video is also neatly done, appealing and can reinforce understanding. I suggest to keep this link in the paper.

See the main PDF for a few parts that need minor adjustments, mostly for improving clarity.

Otherwise, I see a few potential ambiguities that need clarifying:

-Abstract, line 17: you say that the sejugal suture intersects/crosses the metapodosoma in P. wagneri. But later you say that the disjugal suture is probably an apomorphy only present in oribatids. This appears as a contradiction. Should we or should we not consider that a sejugal suture is present in mites other than oribatids? It seems important to clarify this here.

-Your fig. 3B and text indicate that the sejugal suture is not concordant/homologous to the border between prosoma and opisthosoma, and that the metapodosomal-opisthosoma border is somewhere posterior to the sejugal suture in the mites having a distinct sejugal suture. Should you give further considerations for the mites having a clear sejugal suture (e.g. Oribatida), such as explaining that since the homology of the series of c and d setae is established across Acariformes (e.g. oribatids and trombidiforms), therefore it is clear that mites with sejugal suture have their metapodosoma border somewhere between the d and e setae?

If appropriate, there could be a small concluding paragraph, that would include points such as: the Weigman model can be applied to many acariform mites? And what are the main consequences of your finding for taxonomic and/or developmental biology sciences? Is there any consequence other than that segments C-D and their setae, born dorsally (c,d), should be considered as part of the metapodosoma (not the opisthosoma)?

More specific comments:

Line 88: "no real resemblance" is a bit ambiguous, because the sejugal suture is somehow between 2 dorsal humps, therefore it can be percieved/concieved as a furrow, although not intersegmental furrow, based on your findings. So, I suggest to add nuances to your sentence.

Fig 2A: some readers may at first glance wonder if the dorsolateral border of coxal field IV could represent the lower part of the disjugal suture. I suggest to mention these borders (ofboth coxal field III and IV) in your Results to avoid any possible confusion?

Fig 1 caption:

There are 2 E listed. Change the first E for D?

Fig 3 caption. I suggest to add “...for explaining segmentation in elongate...”

**********

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PLoS One. 2022 Feb 25;17(2):e0264358. doi: 10.1371/journal.pone.0264358.r002

Author response to Decision Letter 0

6 Dec 2021

Dear Editor,

Although this is supposedly a letter of rebuttal, I see almost nothing to rebut. I think I have never had such constructive and useful feedback from a pair of reviewers. And although this paper is supposed to require only minor amendments, I found myself having to make some fairly major changes based on the insightful responses of the reviewers (see below).

Best regards,

Sam

-----

Reviewer #1: Arachnids conventionally have a body divided into an anterior prosoma (or cephalothorax) and posterior opisthosoma (or abdomen), but in some groups the two body halves can fuse together to some extent which makes this fundamental division less obvious. The author has submitted an interesting manuscript which goes some way towards clarifying a long-standing problem of how to homologise the (reduced) body of acariform mites with those of other arachnids: in particular where does the opisthosoma begin? The author should be congratulated for producing high-quality images of a soft-cuticled species which I'm sure was challenging to handle, and makes a good case that the leg-bearing segments conventionally referred to as C & D belong to the metapodosoma part of the prosoma. The opisthsoma, in turn, begins behind the segment bearing the last pair of legs as in other arachnids. In this sense the study certainly merits publication and could be suitable for a journal such as PLOS One. However, because its being submitted to a high-profile interdisciplianary journal (and not a specialist acarology publication) I think the manuscript could benefit from placing these results in a slightly broader context, making more comparisons with Arachnida in general. Essentially your data, as I understand it, suggests that the ground pattern of acariforms is a kind of straightforward 4+2 pattern of prosomal segmentation, immediately followed by the opisthosoma. This would make acariforms anatomically similar to things like schizomids, palpigrades and camel spiders (Solifugae). It may be worth noting that at least palpigrades and camel spiders have been proposed, in some phylogenies, as the putative sister-group of acariform mites.

Author: Thank you greatly for this suggestion. This has caused me to make some fairly big changes to the manuscript, and so the paper has been somewhat revamped. I have gone to some effort to expand the model section of the paper in order to broaden the context of the chief finding. I originally had major reservations about extending this model to all arachnids. I am simply not as confident on the rest of Arachnida. But I don’t see that any arachnid deviates from the model that I am proposing. However, if I am going to put this interpretation of the prosoma of mites into the context of all arachnids, I think I have to tackle a misunderstanding that has arisen with respect to the gnathosoma. The circumcapitular furrow is often treated as a segmental border, but this would mean that mites are completely different from other arachnids. This is where I find myself agreeing with van der Hammen. He recognized that the circumcapitular furrow is not a segmental border, which means that the body segments associated with the gnathosoma are not within the gnathosoma itself. And so, I am to some extent according with van der Hammen on the front end of the prosoma, and I am going against him on the back end of the prosoma. Hopefully all of this is a lot clearer in the text while also putting mites into a broader context. I must admit that I have shied away from talking about the phylogenetic significance of a propeltidium, although I accept that there is a fairly high likelihood that Solifugae are sister to either Acari or Acariformes. My general feeling is that this character is too evolutionarily plastic to be very phylogenetically informative for reconstructing phylogenetic relationships among arachnids, especially because it is also found in Schizomida. Although I could discuss these doubts, I would prefer to keep this section as brief as possible because it is side tracking from the main thrust of the paper.

-----

Reviewer #1: As I'm sure the author knows there has also been a long history of mites being described using unique morphological terms, often with limited efforts to homologise them with structures in other arachnids. This hinders comparative morphology, and even phylogeny when homologous characters states are obscured by nomenclature. In the present case, would it be worth expressing the different hypotheses in terms of conventional numbering used in other arachnids? In other words, in the scenario of Weigmann and yourself C and D are prosomal segments 5 and 6, but in the other models they are opisthosomal segments 1 and 2 (or body segments 7 and 8). This could perhaps be done by adding segment numbers to Fig. 1A for example.

Author: This is now addressed in Fig. 1 A–D and in the associated text of the introduction.

-----

Reviewer #1: Related to this, I was thinking to what extent must we seperate dorsal elements from ventral (limb-bearing) elements. In lines 32 you say "There are conflicting interpretations concerning the relationship of these two segments, C and D...to the metapodosoma, which bears legs III and IV." I think what I'm getting at is which segments bear legs III and IV in the Van Der Hammen / Grandjean / Klompen scenarios? It can't be C and D, which they interpret as opisthosomal segments 1 and 2, so what, if anything, did they call the ventral metapodosomal elements bearing the last pair of limbs?

Author: This is now addressed through the same changes mentioned above. The segments bearing legs III and IV are segments V and VI.

-----

Reviewer #1: Another problem is that I couldn't wholly follow how you go from Figure 2A to Figure 3B, with the disjugal suture of oribatids cutting across one (or more) segments of the metapodosoma?

Author: This is now addressed in the second paragraph of the section on the disjugal furrow. The disjugal suture was addressed in lines 88-92 in order to define the difference between a suture and a furrow, but that part is now deleted (see below).

-----

Reviewer #1: You state that P. wagneri lacks a disjugal suture, which I'm sure from your photos is correct. I think the problem lies with lines 88-92 which should include a bit more detail about why the disjugal suture cannot be the typical arachnid prosoma/opisthosoma boundary, and what exactly you mean when you define a suture as something which only intersects a plane. How do you recognise this in actual specimens of mites? You propose that an intersegmental furrow is associated with a narrowing, but (to play devil's advocate) the disjugal suture in your idealised Fig. 3C could be seen as creating a slight fold or narrowing between the regions in front of and behind it. So why is it a suture (other than because of its traditional name?). In essence, your folded suture in Fig. 3B does not look like your smooth suture in Fig. 3A which, if anything, looks more like the prosoma-opisthosoma boundary in 3A.

Author: The other reviewer also picked up on this problem with reference to line 88. I am fond of keeping papers as succinct as possible and dropping concepts and definitions that can come across ambiguously. I am no longer convinced that there is a very robust way of distinguishing a suture from a furrow. There are sometimes humps on either side of a suture, which can make it almost indistinguishable from a furrow. Therefore, I have dropped any mention of suture from the manuscript and simply switched to using the term furrow, which accords with much of the literature. I have made adjustments where necessary. I think the paper is relatively unscathed by this.

-----

Reviewer #1: Also, I did wonder if there is any embryological or hox gene work to support your model? Do the papers by Richard Thomas and/or Austen Barnett help? I recall that they found evidence for only 2 unequivocal segments in the oribatid opisthosoma, but did they indicate where (anatomically) the opisthosoma begins?

https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1525-142X.2012.00556.x

https://evodevojournal.biomedcentral.com/articles/10.1186/2041-9139-4-23

https://www.proquest.com/openview/f22b93c07a71a645657915c444208a67/1?pq-origsite=gscholar&cbl=18750

Author: I have not cited these papers because there is no mention of the chaetotaxy (c, d and e setae). So, they can’t help with the determination of the beginning of the opisthosoma in relation to the rows of transverse setae.

-----

Reviewer #1: Again, the absence of segment numbers (or even the C, D, E scheme) makes it a little hard to follow the argumentation through into the higher oribatids and my question is, in the 3B model where (if anywhere) is the boundary between the segments bearing legs III and IV? The model implies it is not the disjugal suture, as this appears to originate behind leg IV, so have C and D (= 5 and 6) fused together here into an undifferentiated metapodosoma with (in your scenario) the disjugal suture arising as a novel structure and cutting across it?

Author: I have amended Figure 3B and 3C (now 3A and 4B), so that you can see segments C and D, also labelled segment V and VI.

-----

Reviewer #1: The video of the body plan morphing into different hypotheses is nice. I'm not sure how much extra work is involved, but if they colour scheme used in Figure 1 were to be added it would be even clearer where different authors interpreted the start of the opisthosoma.

Author: This is the one place where I feel the need to resist. The video is meant as a standalone piece, largely to encourage people to read this paper. I prefer not to add any more colors, which would complicate it because then I would feel obliged to add a key. It is aimed at the broadest possible audience and is largely designed to give people a first impression about the competing ideas on the segmental homology of mites.

-----

Reviewer #1: May be a formatting problem, but genus and species names need to be italicized here throughout.

Author: Thanks. This should be corrected now.

-----

Reviewer #1: Figure 1: There is no part 'D' in the figure legend, but two part Es. I think it should read "D. Interpretation of Klompen et al. [6]"

Author: Thank you! This has been corrected.

-----

Reviewer #1: Figure 2B: What is being highlighted by the white box? A furrow or protubrence? This is not really explained in the figure legend.

Author: This is now addressed in the caption of Figure 2. My chief concern is that the PDF provides only very low resolution, which may be why this does not seem at all clear. But this should be much clearer in the final publication.

Reviewer #2: I am no expert in arthropod or mite segmentation, but this short paper appears to make a clear point about the need to adjust certain boundaries in body parts, namely the true border between opisthosoma and metapodosoma. The paper is straight to the point, clearly written and fairly strongly argued. The 2 main figures are extremely simple and clear (despite the complexity behind it), and the supplementary figs are also quite useful to support his hypothesis. The video is also neatly done, appealing and can reinforce understanding. I suggest to keep this link in the paper. See the main PDF for a few parts that need minor adjustments, mostly for improving clarity. Otherwise, I see a few potential ambiguities that need clarifying. Abstract, line 17: you say that the sejugal suture intersects/crosses the metapodosoma in P. wagneri. But later you say that the disjugal suture is probably an apomorphy only present in oribatids. This appears as a contradiction. Should we or should we not consider that a sejugal suture is present in mites other than oribatids? It seems important to clarify this here.

Author: Yes, this was awkwardly phrased in the abstract. It is hopefully now amended so that it is clear. Despite extensive searching, I can find no evidence of a disjugal suture in mites outside of Oribatida. I assume that is what is being referred to. A sejugal furrow, on the other hand, is present in many mites outside of Oribatida.

-----

Reviewer #2: Your fig. 3B and text indicate that the sejugal suture is not concordant/homologous to the border between prosoma and opisthosoma, and that the metapodosomal-opisthosoma border is somewhere posterior to the sejugal suture in the mites having a distinct sejugal suture. Should you give further considerations for the mites having a clear sejugal suture (e.g. Oribatida), such as explaining that since the homology of the series of c and d setae is established across Acariformes (e.g. oribatids and trombidiforms), therefore it is clear that mites with sejugal suture have their metapodosoma border somewhere between the d and e setae?

Author: Thanks very much for this suggestion! A new section has been put together to address this, titled “segmental homology”. This is mostly to explain why a single species of mite can be used to determine the true positions of the C and D setae across all Acariformes. The second paragraph addresses this point about the homology of the c and d setae, along with other related points. I think this new version is now much better thanks to this new section. I specifically address how this affects the disjugal suture in the second paragraph of the section on the disjugal suture (please also see the new Fig. 3A).

-----

Reviewer #2: If appropriate, there could be a small concluding paragraph, that would include points such as: the Weigman model can be applied to many acariform mites? And what are the main consequences of your finding for taxonomic and/or developmental biology sciences? Is there any consequence other than that segments C-D and their setae, born dorsally (c,d), should be considered as part of the metapodosoma (not the opisthosoma)?

Author: I disagree with the Weigmann model because there is no warping of the proterosoma. I don’t think that model can be applied to any mites. But the main thrust of this paper was to address where Weigmann was correct. I have now made my position clearer in the model section of the discussion while also emphasizing that the basic arrangement of the body segments of mites is probably the same as other arachnids. This is the main implication of the new model that is proposed in the paper. This model essentially hybridizes Klompen et al.’s interpretation of Acariformes with that of Weigmann. The new model has greater explanatory power because it can be applied to elongate bodied mites. The other two models do a poor job of explaining the large interval between legs II and III. This is now all detailed in the paper. But there are no really important implications with respect to taxonomy and developmental biology other than what is already included.

-----

Reviewer #2: Line 88: "no real resemblance" is a bit ambiguous, because the sejugal suture is somehow between 2 dorsal humps, therefore it can be percieved/concieved as a furrow, although not intersegmental furrow, based on your findings. So, I suggest to add nuances to your sentence.

Author: The other reviewer also picked up on this problem. I am fond of keeping papers as succinct as possible and dropping concepts and definitions that can come across ambiguously. I am no longer convinced that there is a very robust way of distinguishing a suture from a furrow. There are sometimes humps on either side of a suture, which can make it almost indistinguishable from a furrow. Therefore, I have dropped any mention of suture from the manuscript and simply switched to using the term furrow, which accords with much of the literature. I have made adjustments where necessary. I think the paper is relatively unscathed by this.

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Reviewer #2: Fig 2A: some readers may at first glance wonder if the dorsolateral border of coxal field IV could represent the lower part of the disjugal suture. I suggest to mention these borders (ofboth coxal field III and IV) in your Results to avoid any possible confusion?

Author: Amended. Thanks!

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Reviewer #2: Fig 1 caption: There are 2 E listed. Change the first E for D?

Author: Thank you! This has been corrected.

Attachment

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Click here for additional data file. (104.2KB, rtf)

Decision Letter 1

Michael Scott Brewer

9 Feb 2022

Proteonematalycus wagneri Kethley reveals where the opisthosoma begins in acariform mites

PONE-D-21-31633R1

Dear Dr. Bolton,

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Acceptance letter

Michael Scott Brewer

16 Feb 2022

PONE-D-21-31633R1

Proteonematalycus wagneri Kethley reveals where the opisthosoma begins in acariform mites

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Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Fig. Larva FSCA 00030222.

    (TIF)

    Click here for additional data file. (7.1MB, tif)
    S2 Fig. Protonymph FSCA 00030222.

    (TIF)

    Click here for additional data file. (6.8MB, tif)
    S3 Fig. Protonymph FSCA 00030222.

    (TIF)

    Click here for additional data file. (6.5MB, tif)
    S4 Fig. Deutonymph FSCA 00030222.

    (TIF)

    Click here for additional data file. (23.7MB, tif)
    S5 Fig. Adult FSCA 00030222.

    (TIF)

    Click here for additional data file. (20.4MB, tif)
    S6 Fig. Deutonymph FSCA 00030225 (eight minutes after immersion in PVA).

    (TIF)

    Click here for additional data file. (93.7MB, tif)
    S7 Fig. Adult FSCA 00030224 (two minutes after immersion in PVA).

    (TIF)

    Click here for additional data file. (19.6MB, tif)
    Attachment

    Submitted filename: PONE-D-21-31633_MS_reviewer comments.pdf

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    Attachment

    Submitted filename: Letter_of_rebuttal.rtf

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    Data Availability Statement

    All relevant data are within the manuscript and its Supporting Information files. The minimal dataset is the images in Fig 2, which provides all the evidence needed for the discussion.

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