4.1. Phylogeny and Biogeographic History
The quantitative analysis of biogeographic history has advanced tremendously in recent years, e.g., [43
]. However, these methods are yet of little use in studying the history of booids, because Messel is, in a sense, the only booid snake assemblage. To be sure, a large number of fossil booid snake taxa has been described from the Palaeogene of Europe [44
] and North America [46
] and to a lesser extent Africa [47
] and South America [48
]. However, almost all of these taxa are based exclusively on isolated (frequently mid-trunk) vertebrae, and their phylogenetic affinities are therefore virtually unconstrained. To exemplify the problems of phylogenetic interpretation, Smith [49
] studied associated cranial elements and extensive sampling of the entire vertebral column in two late Eocene species from North America, previously considered to pertain potentially to the same genus of ‘erycine’ booid, e.g., [50
]. He showed that these species not only are not ‘erycines’, but they are not even closely related to one another. One, Calamagras weigeli
, is apparently related to the dwarf boa clade Ungaliophiinae, whereas the other, Ogmophis compactus
, is apparently related to the Mexican Burrowing Python, Loxocemus bicolor
]. Since several booid lineages (total clades of Ungaliophiinae, Charininae, Boidae) have their oldest, or near-oldest (if Titanoboa
is a stem boid [51
]), records in Messel, this leads to the appearance that they originated in Europe and dispersed to the New World (or beyond), rather than the other way around. Given the total absence of evidence from North America, and Africa however, this cannot be accepted at face value.
Several of the Messel booid lineages are estimated to have diverged from extant snakes near the Palaeocene–Eocene boundary, coincident with the prolonged period of global warming and hyperthermals around the Palaeocene–Eocene boundary [53
]. Range expansion, as inferred for a number of lizard taxa in North America [38
], could have promoted diversification [54
], especially if accompanied by colonisation of Europe. Regardless, we consider it most probable that Booidea originated in the New World, where the centre of species diversity still lies, and dispersed to Europe, producing the lineages at Messel. Testing that hypothesis will require the discovery of well-preserved early Palaeogene fossils from the New World. The locality of Fossil Lake [55
] as well as rare, associated material from other sites [56
] indicate that this is possible.
Assuming the total clade of Boidae itself has a South American origin, it remains to be established by what route Eoconstrictor
arrived in Europe. Taking into account the long-term isolation of South America from the Upper Cretaceous to the Neogene, two alternative dispersal scenarios can explain our results. A South America-to-Europe dispersal route through Africa, which necessarily entails a transatlantic dispersal, was postulated by various researchers from the Late Cretaceous to the Palaeogene [58
]. The other possibility is a South America-to-Europe route via North America, which is supported by compelling evidence about the faunal dispersal route between North America and Europe during the Palaeogene [61
]. The lack of fossils from Africa and North America with known phylogenetic relations does not allow us to discriminate between these possibilities at present.
4.2. Labial Pits in Extant Snakes
Labial pits are one of the most distinctive features of booid and pythonid snakes, for these organs, together with the facial pits of crotaline vipers, make them capable of perceiving infrared radiation, uniquely among vertebrates. The photons coming from the environment of an animal are a mix of reflected photons, typically in the ultraviolet and visible spectrum, and photons emitted as blackbody radiation, typically in the infrared [65
]. Organs for infrared reception therefore give access to a completely new visual field representing the thermal environment.
The circumoral scales of all examined booids and pythons exhibit specialised receptors called terminal nerve masses, or TNMs [3
]. Each is the expanded, pyramidal terminus, with abundant mitochondria, of the larger branch of the axon of a pseudobipolar neuron whose soma is located in either the ophthalmic or the maxillomandibular ganglion of the trigeminal nerve [3
]. The other branch of the axon of this neuron projects to a specialized part of the myelencephalon called the lateral descending tract and nucleus of the trigeminal nerve, or LTTD [66
]. From there, signals are passed via relays to the optic tectum of the contralateral side (similar to visual signals from the lateral eyes), where they map spatiotopically with signals from the lateral eyes onto the tectal surface [3
]. It is therefore believed that visible light and infrared radiation are integrated into a single ‘broadband’ [3
] image of the environment.
The receptors are exceedingly sensitive, with a rise in temperature of 0.003 ℃ or less capable of producing a signal (modulating the background firing of the neurons) [3
]. The rich capillary beds of the pit organs are thought to help cool the TNMs rapidly and avoid ‘afterimages’ [3
]. TNMs have been documented, and may occur in a concentrated fashion, in the circumoral epithelium of booid species that do not exhibit labial pits, such as Boa constrictor
and Eunectes murinus
]. Indeed, their occurrence is surely responsible for the ability of booids lacking pits, such as the aforementioned species and Lichanura trivirgata
, to perceive radiant energy [23
]. Crucially, however, in pit organs the nerve supply is greater, the receptors more abundant, the capillary network denser, and the epidermis thinner than in surrounding areas [23
]. This is the basis for the correlation we found above between the size of jaw foramina (which carry the branches of the trigeminal nerve as well as the blood supply) and the incidence of pits.
Because the radiant heat receptors and the LTTD are unique to snakes capable of perceiving radiant energy and are present even in species of Booidea lacking pit organs, it is likely that this system was minimally present in the common ancestor of Booidea (and for similar reasons that of Pythonidae). Whether this system is present also in more basally branching taxa such as Xenopeltis
, e.g., [35
], much less other alethinophidian snakes, has yet to be examined. While the ability to sense radiant energy may by itself be advantageous, pits offer further advantages. First, the much greater density of receptors in the fundus (base) of the pit confers greater sensitivity [23
]. Second, because the orifice is always narrower than the fundus, it becomes possible to perceive also directionality and movement [3
]. Yet the distribution of labial pits in Booidea, especially their absence in Boa
, together with the great variability in the number, location and shape of these pits, has suggested that they may have arisen multiple times even in this clade, e.g., [3
4.3. Eoconstrictor and the Evolution of Labial Pits
Fossil evidence bearing on the problem has until now been wanting. The inferred presence of labial pits in Eoconstrictor fischeri therefore gives new insight into their pattern of evolution. First, it shows that a species close to the ancestor of crown Boidae possessed labial pits, making it possible that their absence in extant taxa like Boa and Eunectes represents loss. This would turn the evolutionary question on its head. Second, it shows that the first documented labial pits are located in the upper jaw, rather than in the lower jaw or both simultaneously. Finally, it shows that labial pits evolved very early (in a temporal sense) in the history of Booidea, so that they may have played a larger role in the diversification of the group than hitherto suspected. Until now the timing of their origin has been little constrained.
It is considered that pit organs may confer a selective advantage for different reasons, which may differ depending on the habitat, among other factors. Better visual discrimination of prey has featured most prominently in functional studies [3
]. Clearly, for predators on homeothermic prey (such as mammals or birds) this may be especially important, particularly so if the predator is nocturnal, as may be inferred for Eoconstrictor
given the analyses of Hsiang et al. [35
]. At the same time, it has been demonstrated experimentally that visible light, as opposed to infrared, modalities may dominate in directing prey strikes, and it is likely that both modalities are often used simultaneously [65
]. Other potential selective advantages have received less attention. These include predator avoidance [65
], thermal microhabitat discrimination [3
], and even the selection of ambush sites [71
]. In the latter case, it was considered that the relatively cool background of arboreal perches may assist in the discrimination of flying, homeothermic prey. More generally, labial pits may confer advantages ‘in the general life of snakes … as enhancers of the visual senses of their possessors’ ([3
] p. 293).
As the earliest booid snake in which pit organs have been documented, Eoconstrictor fischeri
illuminates the context in which they arose. The use of pit organs in the detection of homeothermic prey would be a potential function in Eoconstrictor
, but available dietary data are inconsistent with that assumption. The large specimen described by Greene [72
], which in fact appears to be Eoconstrictor
, has a crocodylian, probably Diplocynodon
sp. based on size, in its stomach. (Coils of vertebrae cover the head and tail, so that distinguishing characteristics of the two species [73
] cannot be studied. Furthermore, the plate on which it is conserved is impregnated with fibreglass, so that even high-resolution X-radiographs yielded no insight.) A juvenile Eoconstrictor
had consumed a basilisk lizard, Geiseltaliellus maarius
]. A specimen of a small mammalian carnivore [74
] and a bird [75
] were suggested to have been regurgitated by a large constrictor, but in light of the recognition of a greater diversity of constrictors at Messel, it is unclear to which species these specimens should be attributed. Thus, available direct evidence suggests that poikilotherms were important in the diet of Eoconstrictor
, despite the availability of abundant homeothermic species of appropriate size, such as lipotyphlan mammals [76
] and flightless birds [77
]. Given the extensive behavioural adaptations to maintain a constant activity temperature, it is not out of the question that pit organs are also useful in targeting other poikilothermic amniotes as well. However, Eoconstrictor
does not support the hypothesis that the earliest pit organs were exclusively used to catch homeothermic prey.
The detection and avoidance or deterrence of homeothermic predators is also not supported. Messel is unusual in that large, homeothermic predators are absent from the assemblage [33
]. While this absence might partly reflect a taphonomic filter, it should be noted that large herbivores, especially basal perissodactyls, are abundant [79
]. Furthermore, Mayr [77
] summarised a rich assemblage of flightless birds at Messel, a fact he attributed to an original absence of large terrestrial predators there. Thus, there is no evidence that the labial pits of Eoconstrictor
played a role in the detection or deterrence of homeothermic predators.
Finally, the use of pit organs in arboreal ambush sites is theoretically possible. Flying, homeothermic vertebrates, especially bats, were abundant at Palaeolake Messel [81
]. However, our analysis of habitat preferences suggests a terrestrial way of life, not stenotopically arboreal. Thus, there is no reason to believe that the upper pit organs of Eoconstrictor
were useful in finding such sites (if this were possible [65
]) or catching prey at them. In sum, there is no evidence that the pit organs of Eoconstrictor
played a role in predator–prey relations.
As emphasised by Krochmal et al. [70
], Goris et al. [3
] and others, the ability to sense radiant energy may play many other, less spectacular roles in the life of a snake, and Eoconstrictor
suggests that it is amongst this panoply of possibilities that the functional origin of pit organs within Booidea is to be sought, like, perhaps, the origin of infrared detection itself. At the same time, the advantages noted above that are conferred by pit organs in comparison with mere infrared receptors—the ability to perceive directionality and movement—highlight a conundrum. If Eoconstrictor
did not specialise on homeothermic prey and had no need to avoid large homeothermic predators, then pit organs of the modern type would seem overbuilt. Thus, the limits of our conclusions with regard to the pit organs of Eoconstrictor
should be emphasised. The high density of infrared receptors (TNMs) and vascularisation suggested by our results, which today are uniquely found in pit organs, say nothing about the morphology of those organs. In particular, the soft tissue surrounding the inferred concentrations of receptors is unconstrained, and we do not know the form of the orifice (aperture). In consequence, the extent to which Eoconstrictor
could discriminate directionality and movement is unknown. Finally, we must emphasise again that the number of specimens in which gut contents are preserved is low.
Amongst extant booids (as well as pythons), it is only medium to large-sized species that bear conspicuous pit organs, and they all occupy terrestrial habitats and frequently consume large endothermic prey such as mammals and birds. As our results showed that small booid species from Messel lacked pit organs, they support the existence of a common pattern since the earliest evolutionary history of this clade: pits only occur in larger species. If so, there may exist a noteworthy correlation between size, habitat use and diet that influenced (and still influences) the evolution of pit organs in booid snakes.
Further questions about the origin of the pit organs remain unanswered, such as the importance of their distribution in the circumoral area. Eoconstrictor apparently only had pit organs in the upper jaws, as in extant Morelia viridis, whereas other extant species, such as Antaresia childreni, only have them in the lower jaws. What different roles the exact distribution, not to mention the shape and number, of pit organs might serve in boas and pythons remain unknown.
Although the ecomorphology of Eoconstrictor
could be taken as ancestral for Boidae, caution is yet warranted, given the scant knowledge about other fossil boids. Indeed, if boid affinities and piscivorous feeding ecology of the giant aquatic snake Titanoboa cerrejonensis
from the Palaeocene of Colombia [51
] are confirmed, the ecomorphology and habitat preferences of early boas must have been more diverse than previously thought.