Tadpole Shrimps: Living, Not Fossils

The concept of a 'living fossil' has a fraught history. It tends to appear a lot in popular publications where it conveys a sense of drama and mystery to the organisms so described. In the actual scientific literature, however, it tends to be heavily criticised, due to being poorly defined and of uncertain significance. It commonly gets used to refer to the modern representatives of relictual lineages, often glossing over ways the modern taxa differ notably from their forebears. A reference to 'living fossils' may say more about the writer making it that it does about the intended subject. Consider, for instance, what some have described as the ultimate living fossils: the tadpole shrimps of the Notostraca.

Triops longicaudatus, dorsal and ventral views, copyright Micha L. Rieser.

The tadpole shrimps are a cosmopolitan group of freshwater crustaceans that grow up to ten centimetres in length. They feed on detritus on the bottom of marginal habitats such as temporary pools, brackish lagoons or marshes. Their vernacular name refers to their characteristic body shape, with a flattened oval carapace covering the front of the body (beneath which are concealed the limbs) followed by an elongate, legless abdomen. A pair of compound eyes is visible dorsally near the front of the midline. The body ends in a pair of long caudal rami. Notostracans are a subgroup of the branchiopods, the class of crustaceans that also includes brine shrimps and water fleas. Like other branchiopods, tadpole shrimps have legs with numerous leaf-like branches, adapted for swimming rather than walking. However, whereas many branchiopods have a long pair of second antennae that is used for swimming, tadpole shrimps have both pairs of antennae quite short, presumably in connection with their more benthic lifestyle. The thorax bears eleven pairs of legs, the first of which is elongate and serves to replace some of the sensory function of the rudimentary antennae. The last pair of legs sits on the same segment as the reproductive organs, and in females is modified to form a basket for carrying egs. Like brine shrimps, tadpole shrimps can form a resistent cyst to survive the drying out of their habitat. Also like brine shrimps, this has lead to them being cultured commercially, either as a food supply for fish or as a curiosity in their own right.

Modern tadpole shrimp species are divided between two genera, Lepidurus and Triops, distinguished by the shape of the end of the abdomen. Only about a dozen species are distinguished all up though molecular studies have suggested that there should be more. Notostracans have a sporadic but extensive fossil record, going back as far as the Upper Devonian (Lagebro et al. 2015). And this is where the 'living fossil' concept comes in. The overall form of the tadpole shrimps has been established for a very long time. Indeed, fossils from the Triassic and Permian periods have been described as subspecies of the living Triops cancriformis, which would make it the oldest known species on Earth. Even older fossils from the Carboniferous have been assigned to the genus Triops.

Lepidurus arcticus, copyright Per Harald Olsen.

The problem with these grandiose claims is that their basis is fairly weak. Tadpole shrimps are not heavily sclerotised so their finer features tend to be preserved only rarely. Notostracan fossils often will not preserve much more than the overall proportions of the carapace. And if one wishes to describe Triops cancriformis as a living fossil simply because it has an oval carapace and narrow abdomen, one might as well describe lizards as living fossils because they still have four legs and a tail. A study of the ontogeny of the Triassic 'Triops cancriformis minor', originally described as indistinguishable from the modern species except for its overall smaller size, by Wagner et al. (2017) found notable differences from its modern relative. Both forms have a carapace that becomes longer and narrower over time but, whereas that of T. cancriformis is an oval shape from birth, 'T.' minor begins life rounder and becomes oval with time.

Reconstruction of Almatium gusevi, from Olesen (2009).

One fossil group of crustaceans closely related to the Notostraca is the Kazacharthra, known from the Triassic and Mesozoic of Asia; the two groups have been united in a clade dubbed the Calmanostraca. Kazacharthrans share a number of features with modern tadpole shrimps such as the broad, flattened carapace (albeit one that is proportionately broader than that of Notostraca) and reduced antennae. However, whereas the legs of tadpole shrimps differ from front to back, those of the kazacharthran Almatium gusevi are all similar in structure. In particular, kazacharthrans lack the antenniform first legs of modern notostracans. As it happens, the first legs are also not modified in one Recent species: the little-known Lepidurus batesoni, so far collected once from a location in Kazakhstan (suggesting that the genus Lepidurus is not monophyletic). A phylogenetic analysis of calmanostracans by Lagebro et al. (2015) placed both Almatium gusevi and 'Triops' minor outside the notostracan crown group. It also left open the possibility that 'notostracans', with their much earlier fossil record, are paraphyletic to the Mesozoic kazacharthrans. Lepidurus batesoni was placed closer to other crown notostracans than Almatium or minor, owing to its relatively narrow carapace compared to those taxa and the presence of a rounded anal plate.

So all up, there are problems with describing tadpole shrimps as 'living fossils'. The label focuses on superficial habitus while ignoring the possibility of noteworthy changes in less commonly preserved features. In particular, the antenniform first legs of most modern tadpole shrimps, never yet identified in any fossil species, may be a quite recent innovation. In his 2012 thesis on branchiopod phylogeny, Thomas Hegna ended up concluding that "it seems that Triops cancriformis has no fossil record at all—a dramatic twist of fate for the 'oldest living species'". Hard to qualify as a living fossil when you're not even a fossil!

REFERENCES

Lagebro, L., P. Gueriau, T. A. Hegna, N. Rabet, A. D. Butler & G. E. Budd. 2015. The oldest notostracan (Upper Devonian Strud locality, Belgium). Palaeontology 58 (3): 497–509.

Olesen, J. 2009. Phylogeny of Branchiopoda (Crustacea)—character evolution and contribution of uniquely preserved fossils. Arthropod Systematics and Phylogeny 67 (1): 3–39.

Wagner, P., J. T. Haug, J. Sell & C. Haug. 2017. Ontogenetic sequence comparison of extant and fossil tadpole shrimps: no support for the "living fossil" concept. Paläontologische Zeitschrift 91: 463–472.

The Origins of Song

The world is currently home to roughly ten thousand known species of bird. These come in a significant range of varieties and sizes: ostriches, hummingbirds, penguins, sandgrouse. But one particular clade of birds accounts for roughly half of all living species: the true songbirds of the Euoscines.

Brown treecreeper Climacteris picumnus, a representative of an early-diverging Australian clade of songbirds, copyright Patrick Kavanagh.

Though the name 'Euoscines' doesn't appear to have received a whole lot of usage in the literature, the clade it refers to actually has a long history of recognition. The Euoscines are one of the major subgroups of the well-recognised order Passeriformes, the perching birds. Members of the Euoscines include such familiar animals as finches, crows, wrens, swallows, skylarks, sparrows, and a whole host of others. On a morphological basis, Euoscines are mostly united by the distinctive structure of their syrinx, or voice-box, which is controlled by five pairs of intrinsic muscles (Ericson et al. 2002; by way of contrast, the lyrebirds and scrubbirds that form the clade most closely related to the Euoscines have only three pairs). This complex syringeal structure is doubtless a factor in the elaborate songs that characterise many representatives of the clade and from which the group gets its vernacular name. Molecular data has further strengthened the case for the Euoscines.

Whereas the phylogenetic integrity of the Euoscines is no considered by most researchers to be beyond reproach, its exact origins are a little more mysterious. Outside the Euoscines, the members of the Passeriformes fall into three well supported clades. As noted above, the immediate sister group of the Euoscines is a small Australian clade, the Menurae (the Menurae and Euoscines together form the singing birds, the Oscines). Another very small clade, the New Zealand wrens of the Acanthisittidae, is thought to represent the sister group of all other Passeriformes. The largest clade of Passeriformes outside the Euoscines is the Suboscines, whose members include such examplars as the broadbills and pittas of the Old World tropics, and the antbirds, tapaculos and tyrant flycatchers of the New World. The Suboscines form the sister clade to the Oscines.

Australian logrunner Orthonyx temminckii, another early-diverging exemplar, copyright JJ Harrison.

We also have a fairly clear idea of basal relationships within the Euoscines, primarily from molecular data. I won't dwell on details here (I am aware that while litanies of names can hold a lot of interest for myself, others may find them more tedious) but a detail that has garnered attention is that a preponderance of the basal euoscine lineages are enitrely or predominantly Australasian. This, together with the Australasian distribution of two of the other three major passerine clades, has lead to the proposal that Australasia represents the ancestral homeland for the Euoscines as a whole. But when did the Euoscines first make their appearance?

This is where things begin to get fuzzier. The fossil record of Passeriformes, as for many other birds, is very patchy and often difficult to interpret. Possible passerine bones have been identified from the early Eocene of Australia but they are fragmentary and their identity has been questioned. The earliest well-preserved passerines come from the early Oligocene of Europe (Bochenski et al. 2021). These fossils preserve features indicating that at least the oscine and suboscine lineages had diverged by this time. Attempts to apply molecular dating to the passerine phylogeny, however, have lead to proposals that the major lineages of passerines diverged much earlier, during the Cretaceous era in fact. The divergence of the passerines has then been linked to the break-up of Gondwana, beginning with the isolation of the New Zealand wrens as New Zealand separated from Antarctica about 80 million years ago.

Spotted pardalote Pardalotus punctatus, representing the meliphagoid lineage of Australasian songbirds, copyright Patrick Kavanagh.

Personally, I find this completely incredible. Firstly, it implies a gap of at least 25 million years or so at the beginning of the passerine fossil record (if we accept the Australian fossils as passerines). I've already noted that passerines do not have a great fossil record overall, particularly in the Southern Hemisphere where they are supposed to have originated, but other small birds do have a decent fossil record in the Northern Hemisphere during this time period. The absence of passerines from Europe and North America in the Palaeocene and Eocene does seem likely to be genuine. Secondly, it implies the survival through the devastation of the end-Cretaceous extinction event of not just at least three lineages of passerines but also those bird lineages that diverged before the passerines. At a bare minimum, that requires at least ten clades of birds surviving the Cretaceous and more than likely requires significantly more, most of those lineages also having no recognisable Cretaceous fossil record. Meanwhile, all other non-bird dinosaurs that we do know were around, many of them ecologically very similar, were completely wiped out. Thirdly (and this is perhaps the one that really gets me), it requires that these passerine lineages divided by continental drift then failed to disperse enough over the next eighty million years to obscure the imprint of said drift. Need I remind you that birds can fly? Hand-waving explanations such as the members of many of these early-diverging lineages being poor fliers, or the northern and southern continents being further apart at the time, just don't cut it in my opinion. Why should we assume that if modern Acanthisittidae or Menurae are poor fliers, their extinct relatives also had to be? Eighty million years seems like more than enough time for variation in flight strength to evolve. And a re Suboscines even any more prone to being poor fliers than Euoscines? As for the greater distance between continents, passerines have made their way to isolated oceanic islands (such as those in the mid-Atlantic) that were never close to any landmass. Phylogenetic evidence suggests that some modern passerine groups are indeed the descendants of long-distance dispersals, such as the South American vireos being apparently descended from Asian ancestors, or Hawaiian honeycreepers originating from near the Arctic. And of the previously mentioned European Oligocene passerines, some such as Wieslochia weissi were possibly not part of the Suboscines + Oscines clade (Manegold 2009), indicating that passerines of this grade could indeed make the ocean crossing. So no, the idea of Cretaceous songbirds is just not something I buy right now.

REFERENCES

Bochenski, Z. M., T. Tomek, M. Bujoczek & G. Salwa. In press 2021. A new passeriform (Aves: Passeriformes) from the early Oligocene of Poland sheds light on the beginnings of Suboscines. Journal of Ornithology.

Ericson, P. G. P., L. Christidis, M. Irestedt & J. A. Norman. 2002. Systematic affinities of the lyrebirds (Passeriformes: Menura), with a novel classification of the major groups of passerine birds. Molecular Phylogenetics and Evolution 25: 53–62.

Manegold, A. 2009. The early fossil record of perching birds (Passeriformes). Palaeontologia Africana 44: 103–107.

To Drop Jaw or Not?

The vast majority of living ray-finned fishes (that is, all of them except for bichirs, sturgeons and paddlefishes) fall under the auspices of the clade Neopterygii. I have commented on this clade in earlier posts and in those posts I have noted that modern neopterygians can theselves be divided between three basal lineages. By far the largest of these is the teleosts with only a handful of species representing the other two: the seven or so species of gar in the Lepisosteidae, and the phylogenetically isolated bowfin Amia calva. However, the exact relationships between these three lineages have been the subject of debate.

Close-up on bowfin Amia calva head, from Big Fishes of the World. Note the membranous attachment of the back of the upper jaw.

Historically, the bowfin and the gars were recognised as a group Holostei in apposition to the Teleostei. When first established, this division was motivated primarily by the nature of their scales: the heavy, solid scales of the holosteans contrasted with the thinner, lighter scales of the teleosts. Hence the name 'Holostei' meaning 'entirely bone': the holosteans have both a completely bony skeleton on the inside (as opposed to the partially cartilaginous skeletons of more basal fishes) and a complete covering of bony scales on the outside. However, the heavy scales of the Holostei are a primitive feature, indicating that the two lineages diverged before the evolution of the lighter teleost scales but not indicating a direct relationship with each other.

With the increasing emphasis on evolutionary relationships as the primary informer of classifications, a different system was proposed. This saw the gars as the most divergent lineage of the Neopterygii with the bowfin being united with the teleosts as a clade Halecostomi. This time, the primary evidence for this division was in how their jaws worked. The ancestral condition for vertebrate jaws has them working much as our own still do. The upper jaw, the maxilla, is largely fixed in place against the base of the neurocranium (the brain-holding bit) while the movement of opening and closing the mouth is achieved by the lower jaw, the mandible, pivoting around its hinge towards the back of the skull. In the bowfin and teleosts, however, the maxilla is hinged with the skull at its anterior end and with the mandible at the back. When the mouth opens, the maxila pivots downwards from this anterior hinge, dropping the mandible as a whole downwards. The bowfin and teleosts also possess a bone in the cheek, the interopercular bone, that is not found in other fishes; a muscle attached to this bone rotates the gill operculum as the mouth opens (Lauder 1980). Functionally, the expansion of the mouth cavity in this manner of opening the jaws creates a suction that pulls prey or other food into the fish's mouth.

Though it was by no means universally accepted, it is probably fair to say that the halecostomes vs gars picture of neopterygian evolution became the majority view. But then came the advent of molecular phylogenetic analysis, all ready and willing to cast the proverbial spanner. Rather than confirming halecostome monophyly, molecular analyses pointed the other way, back towards a clade of the bowfin and gars. Following this, a detailed study of gar systematics published by Grande (2010) also supported a gar plus bowfin monophylum on morphological grounds and resurrected the concept of Holostei (albeit redefined on phylogenetic grounds).

Skull of a longnose gar Lepisosteus osseus, from Grande (2010). In the lower diagram, the maxilla is labelled 'mx' and the lacrimomaxillaries are labelled 'lmx'.

Gar jaws, it should be noted at this point, are a bit weird. Rather than being primarily composed of a single maxilla on each side, the upper jaws are made up of a series of tooth-bearing bones, each bone carrying just a few teeth, that have been dubbed the lacrimomaxillaries. When the jaws open, as well as the lower jaw opening in the standard manner, the flexible upper jaw also bends upwards. Rather than using suction to draw in their food like other neopterygians, gars capture prey by sneaking up to it then using a quick sideways jerk of the head to bring the open jaws around the prey (Lauder 1980). Gars were excluded from the Halecostomi on the basis of their lack of a long, mobile maxilla but, as explained by Grande (2010), a mobile maxilla is indeed present in gars but reduced to a remnant splint at the back of the jaw (in mature alligator gars Atractosteus spatula, the maxilla does not ossify). In very young juvenile gars, the mobile maxilla remains a significant part of the upper jaw with the lacrimomaxillaries being added in front of it as the jaw lengthens. As for the interopercular, this is genuinely absent in modern gars but it is present in close fossil relatives of gars such as semionotids. Rather than retaining a primitive jaw structure that was superseded in the bowfin and teleosts, it appears that gars evolved their own derived jaw structure from 'halecostome' ancestors.

Given that suction-assisted feeding is generally regarded as a major advance in fish evolution, how did gars end up abandoning it? That I can only speculate about. Is it related to the evolution of their elongate rostra? Long beaks are certainly a thing for a number of teleosts, but I don't know if any have a beak as long and robust as a gar's. Could it be that the greater precision of gars' snapping mode of feeding is an advantage in the low-oxygen, muck-filled waters in which gars thrive? Or could it be a side effect somehow of gars' more heavily armoured condition than other early-diverging neopterygians?

It's only fair to note that monophyly of Holostei is still not universally accepted; there are sill researchers who are inclined to think the bowfin closer to teleosts. But even if the 'Halecostomi' hypothesis was to rise once more to the surface, it would not be for the same reasons it did before.

REFERENCES

Grande, L. 2010. An empirical synthetic pattern study of gars (Lepisosteiformes) and closely related species, based mostly on skeletal anatomy. The resurrection of Holostei. Copeia 2010 (2A): iii–x, 1–871.

Lauder, G. V., Jr. 1980. Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus, and Amia. Journal of Morphology 163: 283–317.

Tears of a Baby

For many people, the most familiar members of the plant family Urticaceae are the stinging nettles. However, the nettles make up only one part of this cosmopolitan family and there are many representatives that do not sting. One such plant is Soleirolia soleirolii, commonly referred to by the vernacular name of baby's tears.

Baby's tears Soleirolia soleirolii growing around dwarf horsetail Equisetum scirpoides, copyright Carnat Joel.

The only species of its genus, Soleirolia soleirolii is a small creeping herb with more or less succulent stems and subcircular leaves half a centimetre or less in diameter (Harden 1990). It grows in damp habitats and may even grow submerged in water. Baby's tears form a dense flat mat with stems rooted at the nodes. The tiny white flowers reach only a millimetre in size. Wikipedia lists a number of vernacular names for this plants, such as baby's tears, angel's tears, Corsican creeper, or mind-your-own-business (I have no idea what this last name refers to).

In its native range, Soleirolia soleirolii is mostly restricted to islands of the western Mediterranean, including Corsica, Sardinia and Majorca, with a localised mainland population near Rome in Italy (Schüßler et al. 2019). A population was also recently discovered near the coast of Algeria (Hamel & Boulemtafes 2017). On the basis of molecular phylogenetic dating, Schüßler et al. (2019) suggested that its current range may be relictual, having gone extinct over most of mainland Europe as the climate changed. However, as those who glanced at the references for this post may have already guessed, Soleirolia has now become established in many parts of the world outside its native range. It has often been grown as a ground cover or houseplant. If it finds itself somewhere it likes, it may become invasive; though easily uprooted, its proclivity for vegetative reproduction means that it can easily return if not thoroughly cleared. And so we have a paradox, where what is regarded as a valuable relict in one location may be considered a vexatious weed in another.

REFERENCES

Hamel, T., & A. Boulemtafes. 2017. Découverte d'une endémique tyrrhénienne Soleirolia soleirolii (Urticaceae) en Algérie (Afrique du Nord). Flora Mediterranea 27: 185–193.

Harden, G. J. (ed.) 1990. Flora of New South Wales vol. 1. New South Wales University Press.

Schüßler, C., C. Bräuchler, J. A. Reyes-Betancort, M. A. Koch & M. Thiv. 2019. Island biogeography of the Macaronesian Gesnouinia and Mediterranean Soleirolia (Parietarieae, Urticaceae) with implications for the evolution of insular woodiness. Taxon 68 (3): 537–556.