Two different forms of cryptic species-complexes in mites of the Histiostomatidae (Astigmata) from bank mud and bark beetle-galleries and their significance for applied biodiversity research
SEM objects (sputtered with gold) , SEM photographs and light microscopic slides of the named species of Histiostomatidae are part of my private collection. An adult specimen of H. maritimum from the same population in Berlin, but collected earlier during my diploma thesis is located in the collection Dr A. Fain, cabinet 3, box 136 under slide number 50a, now belonging to the collection of the Royal Belgian Institute of Natural Sciences.
a) Evolutionary context
It cannot be decided by an absolute definition from when on, similarities of species suitable for confusion must be designated as cryptic. Using suitable modern methods, cryptic types can always be distinguished, provided that they are actually different species. The terminology of the cryptic species complex can therefore not be a concept that is clearly determined by natural phenomena. A precise definition established by scientists does not make sense either. I therefore agree with Korshunova et al. (2019) that the concept of cryptic species complex is not absolutely necessary in order to work profitably taxonomically with species that are very similar to one another. It is also a question of the point of view, whether one is a specialist in a group of organisms or not, to designate even larger taxa as cryptic groups without revealing oneself as laypeople. Compared to the morphological diversity of other mite taxa, such as the paraphyletic Oribatida, the mites of the Histiostomatidae have essentially remained a fairly uniform construction plan (e.g. Wirth, 2004).
I therefore regard the terminology of the cryptic species complex as more of a practical working concept.
The knowledge of numerous species complexes with very similar morphology within a taxon allows the specialists for this taxon to conclude, for example, whether the known number of species is far below the actual number of species or not. Within the mites of the Histiostomatidae I assume a greatly underestimated biodiversity. This is not only due to the fact that cryptic species groups may initially only be assigned to one species, as shown, for example, for strains that look similar to H. feroniarum (Witalinski et al. 2014), but in this case also to the fact that there are too few researchers, who systematically examine habitats suitable as habitats for such mites.
Conversely, there is of course always the possibility that supposedly several species will turn out to be subspecies of a single species. For example, Neanderthals and modern humans were earlier considered to be members of one species despite their gradually different morphology, until molecular biological comparisons justified two different species (e.g. Paixao-Cortes et al., 2012). Afterwards, more detailed morphological investigations, e.g. the nasal complex (Marquez et al., 2014) support this more modern thesis. However, the thesis is called into question again, for example, by works such as Hajdinjak et al. (2021), according to which modern humans of the Palaeolithic also had Neanderthal ancestors.
In most organism groups, however, the variant of an undetected higher species diversity predominates over the opposite option, such as the discovery of the monitor species Varanus ornatus (e.g. Böhme & Ziegler, 2004) or the characterization of a new mite of the Histiostomatidae based on ultra-structural studies (Witalinski et al., 2014).
In addition to various aspects of biodiversity research, cryptic species groups (monophyletic or non monophyletic) or cryptic sister species (= sibling species) are also of interest from an evolutionary perspective (e.g. Bickford et al., 2007).
Particularly meaningful cases are those, in which the assessment of whether or not there is a specific species status, such as in the case of the Neanderthal men, fluctuates back and forth.
In the case of closely related species, for which the species concepts, in particular the eco-species concept, cannot yet be assessed strictly enough, it can be assumed that the event that gave rise to two species from one population happened not very long ago in geological terms. In the case that the recent populations are not yet sympatric, but can still be found in adjacent distribution areas, an allopatric speciation can often be reconstructed. An example are the yellow-bellied toad Bombina variegata and the red-bellied toad Bombina bombina, the evolution of which can be traced back to the last ice age barriers (e.g. Gollmann, 1984).
There is only one hybridization zone beyond which neither hybrids nor the respective parents spread further, since the formation of niches is still too similar to competition, resembling still an intraspecific level.
This concept for assessing an age tendency of closely related species can also be applied to those mites of the Histiostomatidae presented in this work. H. maritimum, H. litorale, H. palustre and H. sp., however, represent seemingly by no means a separate monophyletic group.
Although the existence of a cryptic group of species indicates a very close phylogenetic relationship, monophyly does not have to be given (I refer here to a general aspect of the phylogenetic systematics). Instead, the species in question can also be paraphyletic. There is also the possibility that within a group of similar species those species that occur sympatricly in an examined habitat are polyphyletically distributed. According to Wirth (2004), this is possible and is based on a phylogenetic tree with more or less gradual morphological characteristics for the species H. maritimum, H. litorale and H. palustre. According to this tree, H. litorale is established as a possible sister species of H. palustre, while H. maritimum is assumed to branch off the Histiostoma feroniarum-group elsewhere. H. sp. was not yet known at the time. Since it was only found years later, after the study area had changed significantly from an ecological point of view, it is also unclear whether it still occurs sympatric with the above-mentioned species, as these could no longer be found.
The relationship between the three cryptic species mentioned above can best be explained descriptively. A term such as „species flock“ is not applicable to these three species, nor to the Histiostoma feroniarum-group. Although Hodges et al. (1994) expanded the term for widespread species, but in this case the Histiostoma feroniarum group seemingly also lacks monophyletic character. According to Wirth (2004) it is probably paraphyletic.
Since H. maritimum, H. litorale and H. palustre appeared sympatric in the study area and, according to Scheucher (1957), the first two species can even share numerous phoretic hosts, I assume that they are phylogenetically/ geologically older species.
Because the species are obviously compatible with each other in the same habitat and in the same substrate and partly in their phoretic words. The niche formation is diverse enough that competition is avoided.
This is also to be seen morphologically in the three species discussed here, since the cryptic aspect only affects the deutonymphs. This indicates that in their evolution different strong selection pressures acted on deutonymphs and free-living stages (here adults).
In general, for species that are very similar to one another, a low level of morphological/genetic variation suggests a rather rapid and not so long ago radiation (e.g. Hodges et al., 1994). However, the morphologically very different adults of the mite species in question do not support this thesis. I therefore assume that the species of the Histiostoma feroniarum-group could afford to keep an old blueprint in the deutonymphs for a longer period of time, since the crucial ecological licenses for niche formation within the muddy habitat had an effect on the free-living stages and less on the conditions of the phoretic stage on its hosts.
Accordingly, it is not a question of how a deutonymph from this H. feroniarum-group group can avoid competition with any other species of the same group on the same host, but rather all is about when leaving the host: namely at different times under different ecological conditions (or, as in the case of necromance, on the host to stay until his death). It is assumed according to Wirth (2004) that the development of the three species (plus H. sp.) in sapropel around standing waters has evolved at least twice convergently within the paraphyletic taxon called „H. feroniarum group“. I also include the fact that the free living instars of the necromenic H. maritimum are also temporarily available in the mud, moving around the carcasses of their hosts.
To determine the age of a taxon, it is helpful to include fossils in the reconstructions. Fossils of mites are rarely found in sedimentary deposits, but often in amber. However, such amber is rarely scientifically examined, which is why, for example, knowledge of fossils of the Histiostomatidae is very sketchy. However, according to Dunlop et al. (2011) the minimum age of mites of the Histiostomatidae is 40-50 million years. Mites of this morphological design therefore already existed in the Eocene. While no fossil record is known from the closer relationship of Histiostoma maritimum, a representative from the distant relationship of H. piceae from Baltic amber is known and assigned to the bark beetle-clade on the basis of its deutonymph morphology (Wirth & Garonna, 2015). This deutonymph, which attached to the body of a bark beetle of the genus Phloeosinus, is also settled in the Eocene with an approximate age of 44-49 years.
In my recent research I use to name different clades within the bark inhabiting histiostomatid mites (Wirth, 2004), a larger taxon with mite species that generally inhabit bark, which I consider monophyletic. I consider the bark-beetle clade (Wirth & Garonna, 2015) as a monophyletic subgroup, a group that appears in my older tree (Wirth,2004) as a sister group relationship of the Histiostoma piceae-group and the Histiostoma dryocoeti-group (the latter names follow Scheucher, 1957 ). The bark beetle-clade has common morphological features of the deutonymph and the mouthparts of the adults. The mites are associated with bark beetles of the Scolytinae (there are exceptions). One sub-clade is the already mentioned Histiostoma piceae-group, which is characterized by having a H. piceae-like deutonymph. The H. piceae-group is larger than expected by Scheucher (1957). But the group name itself is recently also adopted by other authors (Khaustov & Klimov, 2018).
Based on the species H. piceae, H. ulmi and H. scheucherae, a cryptic group of species is herewith emphasized for the first time, which is phylogenetically arranged „around“ H. piceae. I consider this group to be monophyletic based on the dorsal morphology of the females (presence and arrangement of specific humps). I assume that even several species more will be assigned to this group in the future. This cryptic group could for example be referred to as Histiostoma piceae sensu lato (e.g. Wallis et al., 2001). An alternative designation could be H. piceae species flock (e.g. Hodges & Arnold, 1994).
The two above mentioned amber fossils prove that the Histiostomatidae already underwent greater radiation in the Eocene and developed more specific phoretic relationships, such as bark beetles of the Scolytinae.
Due to the morphological similarities of the members of that bark beetle-clade, it can be assumed that radiation occurred rather quickly in that distant geological period.
The long phase of evolution of the bark-beetle-clade mites with bark beetles (Scolytinae), raises the question of coevolution between Phoronts and hosts.
Phylogenetically comparative studies on the possible coevolution between mites of the bark-beetle clade and the Scolytinae do not yet exist. However, the hosts of H. piceae, the bark beetle sister-clade with Ips typographus and I. cembrae (Wirth et al., 2016), might indicate parallel evolution, at least at the level of these two phoretic associations. Coevolution assumes that there is a selection pressure in one partner of an organism-association (like parasitism or phoresy) to survive with the other. According to van Valen (1973), evolutionary optimizations of one species lead to a competitive advantage over the other, and it can thus take up a larger proportion of available resources. An understanding of possible coevolutionary processes, e.g. between H. piceae and its bark beetles, however, requires that the biological relationships between phoront and host be better understood. However, it is largely unknown what role, for example, the mite plays in the bark beetle’s galleries. Khaustov & Klimov (2018) formulate the thesis for members of the Histiostoma piceae-group generally that the mites hyperphoretically introduce fungal spores into the bark beetle galleries, some of which serve the mites as food after the fungus has germinated, which might additionally harm the corresponding tree as well as the host’s brood. Fungicidal glandular secretions from the mites would cause the fungal growth to be inhibited, which is why the rudimentary hyphae could more easily be incorporated through the filtering apparatus of the mite’s mouthparts.
I assume that the mite-fungus-host correlation is more complex, as the fungicides of the opisthonotal glands might additionally cause more hygienic conditions in the bark beetle galleries, what could be even beneficial for the brood. A balance between the total elimination of fungi that are harmful to the host’s brood and the only reduction of a forage fungus, which then even might damage the brood, can depend on as yet unknown conditions. In Wirth & Moser (2008), for example, I observed the mite Histiostoma bakeri occuring mainly in the detritus chambers of the ant Atta texana and there seemingly creating a hygienic advantage for the host.
Since the three species from the Histiostoma piceae-group named here are difficult to distinguish in all stages and therefore form a cryptic group of species according to the conventional definition, a rather younger age of this complex can be assumed. The assumed host specificity of the concerned mite species does not contradict this thesis, since according to Jaenike (1993) it could be shown experimentally on parasitic nematodes that host specificity can evolve very quickly.
It is interesting that of the three mite species discussed here, only one, namely H. piceae, is phoretically bound to beetles of the Scolytinae, while (according to Scheucher), H. ulmi and H. scheucherae share the same host of the Tenebrionidae, Hypophloeus bicolor (= Corticeus bicolor). The same principle applies here, as I assumed for H. maritimum and H. litorale: what matters is that the phoretic host is left under different conditions. While H. ulmi develops in beetle galleries, H. scheucherae needs sap flux for further development.
I assume that the last common ancestor of the three cryptic mites had a bark beetle host of the Scolytinae and that this stem species showed biological similarity to H. piceae. Because H. piceae is noticeable under laboratory conditions as well as in the original substrate due to the following peculiarity: the species can reproduce very rich in individuals even under natural field conditions. If at some point a specific number of deutonymphs have been formed, in addition to the actual host, they also apparently randomly occupy other arthropods that are in the galleries of the Ips species, such as mite species of the Parasitiformes (regular own observations, not yet explicitly published). However these arthropods are mostly unsuitable for a successful dispersal of H. piceae. But the behavior shows that a permanent horizontal transfer from a H. piceae-like mite associated with Scolytinae to a non-Scolytinae host such as Hypophloeus bicolor, which is a predator in Scolytinae galleries in search of bark beetle larvae, is easy to imagine.