Lampreys underwent radical changes in ecology and morphology during the Jurassic era

doi:10.21203/rs.3.rs-2414749/v1

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Lampreys underwent radical changes in ecology and morphology during the Jurassic era

https://doi.org/10.21203/rs.3.rs-2414749/v1

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published 31 Oct, 2023

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Lampreys, the oldest living jawless vertebrates, represent an iconic model in evolutionary biology and are always intriguing for their bizarre feeding behavior of sucking blood or gouging out tissues from their victims. They seemingly underwent few changes in morphology and feeding habit since their first appearance in the Late Devonian. However, their evolutionary history is not so simple, as demonstrated by two superbly preserved large lampreys from the Middle-Late Jurassic Yanliao Biota of North China. These fossils present radical changes in the feeding apparatus, body size, and life-history strategy of their group during the Jurassic era and paved the way for the origin of living lampreys. Their extensively toothed feeding structures are radically different from the simply structured dentition of their unusually small-sized and probably non-predatory Palaeozoic relatives but surprisingly resemble the Southern Hemisphere pouched lamprey, which foreshadows an ancestral flesh-eating habit for modern lampreys. In the petromyzontiform timetree recalibrated on the basis of these stem lampreys, the evolutionary increase of lampreys’ body size accompanied the establishment of the modern-type three-phased life cycle, which was likely triggered by the concurrent evolutionary thinning of the body integument of their most significant piscine hosts in the Early Jurassic. Our study also places modern lampreys’ origin in the Southern Hemisphere of the Late Cretaceous, followed by an early Cenozoic anti-tropical disjunction in distribution, hence challenging the conventional wisdom of their biogeographical pattern arising from a recent origin in the Northern Hemisphere or the tectonic fragmentation of Pangean supercontinent as far back as 200 million years ago.

Biological sciences/Evolution/Palaeontology

Biological sciences/Zoology/Ichthyology

Biological sciences/Ecology/Biogeography

As the representative lineage of the living jawless vertebrates, lampreys have great weight in the study of vertebrate evolution. They are always intriguing because of their bizarre feeding behavior of sucking blood or gouging out tissues from the prey to which they firmly attach thanks to their toothed oral sucker^1–7. They have been in existence for ca. 360 million years but left an extremely patchy fossil record in the post-Carboniferous period, with only one species known from the Cretaceous^2,4,8. Despite the superficially conservative adult morphology throughout their history, from the simply assembled analogue in Palaeozoic fossils, lampreys’ feeding mechanism, especially the size, shape and arrangement of the keratinous teeth had been substantially reformed and enhanced to the pattern of modern species^2,4,7–11. And evidently, departing from their Palaeozoic kins with non-ammocoete larvae and expanding the habitats to the freshwater domain, lampreys had renovated the life-history strategy some time before the Cretaceous by evolving the ammocete and metamorphic stages^4,8,12. Thereafter they established their current diversity and anti-tropical distribution^5,6. However, these scenarios were so poorly understood due to the lack of reliable fossil record and the disputed lamprey phylogeny, especially that of the crown-group lineages^1–6,8. Here we shed light on these questions by reporting two lampreys from the Jurassic terrestrial fossil Lagerstätte Yanliao Biota of North China¹³. These fossil lampreys were exquisitely preserved with a complete suite of feeding structures, including the well-developed biting plates on the piston-like tongue, which has been never seen in previously known fossil lampreys and astonishingly resembles the pouched lamprey now confined to the Southern Hemisphere. Bridging the recorded fossil and extant lampreys, these new fossils offer an opportunity to reconstruct the evolutionary process and the ancestral state of modern lampreys’ feeding mechanism. As key constraints of the evolutionary timeline of its group, they also make it possible to assess the coevolutionary interactions with the potential hosts and the consequent implications to the establishment of the modern-type life history mode of lampreys. Also, based on the renewed lamprey crown-group phylogeny, the early biogeographical history of modern lampreys was reconstructed and their ‘poles-apart’ distribution pattern was reinterpreted.

Systematic Palaeontology

Class Cyclostomi

Order Petromyzontiformes (Hyperoartii)

Genus Yanliaomyzon gen. nov.

Type species. Yanliaomyzon occisor gen. et sp. nov.

Diagnosis. Stem lampreys with relatively small oral disc but strongly-developed keratinous dentition; posterior disc and circumoral teeth lacking, anterior and lateral circumoral teeth spatulate in shape and each bearing three convergent blades; supraoral lamina large and consisting of two stout central cusps flanked by wing-like lateral extensions; transverse lingual lamina very large with the apice of its tripartite cusps interlocking with the supraoral lamina.

Included species. Yanliaomyzon ingensdentes gen. et sp. nov.

Etymology. ‘Yanliao’, derives from Yanliao Biota, a Jurassic terrestrial Lagerstätte from North China¹³, where these fossils were discovered; ‘myzon’ (Greek), sucker.

Yanliaomyzon occisor gen. et sp. nov. (Figs. 1a–e, 2d, f, Extended Data Figs. 1g–i, 2a–g, k, l)

Etymology. Latin ‘occisor’, meaning ‘killer’, refers to the powerful hunting skill of the species.

Holotype. IVPP V 15830, a completely-preserved lamprey.

Paratype. IVPP V 18956A, B, a lamprey with the head and anterior trunk preserved.

Horizon and locality. Tiaojishan Formation, Oxfordian, earliest Late Jurassic; Bawanggou, Mutoudeng Town, Qinglong County, Hebei Province, China, ca. 158 million years ago (Ma)¹⁴.

Diagnosis. The supraoral lamina spanning completely the lateral rims of the oral aperture; body very slender with tail region occupying ca. one fourth of total body length.

Yanliaomyzon ingensdentes gen. et sp. nov. (Figs. 1f–h, 2a–c, e, Extended Data Figs. 1a–f, 2h–j)

Etymology. Latin ‘ingens + dentes’, meaning large teeth, refers to the large cuspid laminae on the rasping piston.

Holotype. IVPP V16715A, B, a completely preserved individual.

Paratype. IVPP V 16716A, B, an exquisitely preserved toothed oral disc and the laminae on the tongue.

Horizon and locality. Daohugou beds (late Middle Jurassic, ca. 163 Ma) (personal communications to Z. Q. Yu) in Wubaiding Village, Reshuitang County, Liaoning Province, China.

Diagnosis. The supraoral lamina occupying roughly one third of the rim of oral aperture; body relatively deep, the dorsal fin contiguous with the high and large anterior caudal fin, the tail occupying more than 40% of total body length.

Description and comparison:

Yanliaomyzon igensdentes and Y. occisor are fairly large (Supplementary Table 1) with the latter (> 700 mm) being among the largest of the group, only slightly smaller than the anadromous sea lamprey Petromyzon marinus and Pacific lamprey Entosphenus tridentatus^5,11.

The most conspicuous features of these species are the extensively toothed oral disc and piston-like tongue (Figs. 1, 2a–f, Extended Data Figs. 1b–d, h, i, 2h–l). Their dentitional arrangement, similar to one another in general morphology, strikingly resembles that of pouched lamprey Geotria australis (Fig. 2g) currently distributed in Southern Hemisphere^9,10. Their relatively small oral discs occupy 4.8% and 6.7% of the total body length in Y. occisor and Y. ingensdentes, respectively, approaching the condition of modern flesh-eating lampreys¹⁰. The closely arranged disc teeth are dorsally flattened, slightly concave in the posterior surface with the blade-like dorsal edge pointing towards the center of the oral aperture. Posterior disc teeth and circumoral teeth are lacking. The circumoral teeth are spatulate in shape with the longest of the three converging blades facing slightly sideways. By analogy, this arrangement of these structures might function similarly as their counterparts of Geotria in allowing the forward sliding of the oral disc over the host and resisting any tendency to slip backward or laterally, thereby coordinating the biting movement of the transverse lingual lamina^9,10. The supraoral lamina is very large and has a pair of central inner cusps flanked by a pair of large and curved wings as in Geotria⁹. The wide infraoral lamina is surmounted by a straight row of about ten stout cusps. The transverse lingual lamina is remarkably large and occupies most of the part of the oral aperture (Fig. 2a–f, Extended Data Figs. 1g–i, 2h–j). This lamina is thus proportionally much larger than that in living lampreys^10,11, whereas this structure is likely much less developed, if present, in all other known fossil lampreys^4,8,15–21. This toothed lamina is convexly curved and characterized by a prominent central cusp flanked by two slightly smaller lateral cusps like in Geotria^9,10. The tips of its tricuspid cusps, when raised upwards in life, interdigitate with the grooves on the rear side of the supraoral lamina (Fig. 2a–f), which, again, recalls the feature unique to Geotria among living lampreys and allows powerful biting and removing large amounts of flesh from the prey^9,10.

The prebranchial region is longer than the branchial apparatus (Fig. 1c–e, f, h). The eyes are medium-sized, with the otic capsules positioned immediately behind (Fig. 1c, d, f). The gular pouch of these lampreys (Figs. 1b, e, 2a–c, e, f, Extended Data Fig. 2h–l) is small and seemingly has two lumina (Fig. 1b, 2a–c, e, f). This structure was also observed in the Cretaceous lamprey Mesomyzon mengae⁸but never seen in any other fossil lamprey^4,15–20. Where present, this structure in pre-spawning and spawning males may have the function of courtship display or energy storage for spawning migration for anadromous species²². Five out of nine living lamprey species with gular pouch are anadromous^{11, 22}.

The dorsal fin of Yanliaomyzon is fairly long and extends anteriorly until the level of the fourth gill pouch (Fig. 1c–e, f, h) as in Mesomyzon mengae⁸. Before the cloaca, a long preanal skin fold is developed in both species and extends anteriorly to the anterior branchial region (Fig. 1c–e, f, h).

In the position of the intestinal duct several tooth-bearing jaw bones and possibly skull bones of some unidentified bony fishes and some skeletal relics are preserved in Y. occisor (Extended Data Fig. 2a, c–f) and Y. ingensdentes (Extended Data Fig. 1a, f), respectively.

Phylogenetic analyses

Different from previous analyses^4,23–27, our study includes the revised data of Mesomyzon and takes the full use of data (including the morphological characters, molecular sequences and fossil ages) in an integrative way (Method in Supplementary Materials). The all-compatible consensus tree shows that within the cyclostome monophyly and crownward to the basal Palaeozoic lampreys, three Mesozoic species, Mesomyzon mengae, Yanliaomyzon ingensdentes and Y. occisor were positioned successively along the stem, with the latter two immediately basal to crown-group lampreys (Fig. 3). In the revised crown-group intrarelationships, Geotria (Geotriidae) was for the first time resolved as the earliest diverging lineage, sister to the pair of Mordacia (Mordaciidae) and Petromyzontidae. These memberships are radically different from those inferred in other previous studies^4,23–27, which either supported Geotriidae-Mordaciidae²³ or Geotriidae-Petromyzontidae pairs^26,27, or their interrelationships were unresolved in a basal polytomy^4,25. Calibrated by the new fossils, some key divergence times in petromyzontiform’s history were reset. Mesomyzon, the earliest lamprey with modern triphasic life history known so far^4,8,12, diverged from the stem in the late Early Jurassic (95% HPD: 236.0-163.00 Ma; median: 181.8 Ma). The petromyzontiform crown was estimated to originate in the Late Cretaceous (Campanian) (95% HPD: 122.7-40.8 Ma; median: 78.0 Ma), which is roughly 90 million years (Myr) younger than the recent total-evidence inference (169.82 Ma)²³and roughly 240-97 Myr younger than previous molecular-dating estimate (280-220 Ma)²⁴, respectively. Within the crown, the split of Southern and Northern Hemispheric lampreys was estimated to occur in the late Palaeocene (95% HPD: 95.0-29.5 Ma; median: 58.6 Ma), which is again much younger than aforementioned estimations^23,24. The Northern Hemispheric lineages were estimated to diversify since the late Oligocene (25.7 Ma), much younger than the previous total-evidence dating(ca. 70 Ma)²³but compatible with that based on nuclear data alone (40-10 Ma)²⁴.

Feeding mode, life history and swimming performance of Yanliaomyzon

Yanliaomyzon species’ dentitional arrangement, and the stomach content point to the flesh-eating habit. Their dentitional pattern resembles Geotria, a large, monstrous flesh eater that can even destroy the skull of teleost fish²⁸. The phylogenetic distribution of the feeding modes suggests that the flesh-eating habit should be ancestral for modern lampreys, rather than the blood sucking as traditionally noted^10,28.

Yanliaomyzon occisor, the largest fossil lamprey known so far, ranks among the largest in modern species^5,11. Living lampreys’ adult body size is intrinsically related with their key biological features, with the larger and predaceous species capable of migrating farther and achieving wider distribution, laying much more eggs, and more tolerant to salt waters⁵. In body length, Yanliaomyzon occisor falls within modern anadromous lampreys but notably departs from the smaller freshwater residents and non-feeding forms⁵. This implies for the anadromy wherein the higher marine productivity could have provided more feeding opportunities and hence greater growth potential. Being phylogenetically bracketed by Mesomyzon and modern lampreys, which all have a triphasic life cycle, Yanliaomyzon species could likely have also evolved this strategy, given that the acquisition of this trait is probably irreversible in lampreys²⁹.

Yanliaomyzon species, like Mesomyzon, also have an extraordinarily long-based dorsal fin and a ribbon-like preanal skin fold that considerably extends the lateral side of the body and thus facilitates the power transmission to the water during swimming³⁰. As shown in living eels and African knifefish (Gymnarchus niloticus) with similar body plan, these vertical stabilizer structures represent an adaptation of swimming in high hydromechanical efficiency^30,31, which is especially significant in the upstream migration and long-distance dispersal.

The evolution of lampreys’ feeding structures and its implications

Regarding the evolutionary rates of the feeding mechanism, the Mesozoic species act as the ‘watershed’ in the history of lampreys. The relative rates along the branches downward and crownward to themselves greatly differ, with the former almost ten times the latter (Extended Data Fig. 3). The crown-group lampreys show a rather low rate when they depart from Yanliaomyzon in the Late Jurassic, and then have very uneven rates in their later history, with the rate at the branch subtending Mordaciidae and Petromyzontidae ca. 77 times that low rate towards Geotriidae. These reflect the novelties of the feeding mechanism in the Mesozoic lampreys relative to the Palaeozoic species and highlight the marked reinforcement of those Geotria-like biting structures in Yanliaomyzon, which approximates the state of the most recent common ancestor of crown-group lampreys.

As indicated by the lineage of Mesomyzon, the substantial shift of the life history from the ancestral type⁴ to that comprising three phases might have occurred no later than the late Early Jurassic (ca. 180 Ma) (Fig. 3). This ‘jumping-off point’ appears to coincide with a dramatic evolutionary increase of the body size of these animals, which should be historical products of the enhancement of the feeding structures and the emergence of plenty of suitable host species. The Palaeozoic lampreys are all very small and lack an ammocoete phase⁴, which should be associated with their simply structured dentition and the limited buccal cavity, the space accommodating the anti-coagulant secreting glands and food processing⁷. Their buccal cavity is squeezed by the anteriorly positioned branchial region, which culminates in Priscomyzon whose first two gill pouches even extend anterior to the eye⁴. Those early lampreys’ oral disc and associated structures all point to the enhanced attaching capability, but the real ‘biting’ structures, i.e., those laminae on the rasping piston were so weakly developed that they were never preserved or unrecognizable in the fossils despite the clearly observable circumoral teeth⁴. Moreover, were they predatory forms, their feeding opportunities were rather limited because the vast majority of their potential hosts then all had thick scales surfaced by enamel or dentine layers or ridges³², thus too hard for them to bite. Actually, the oral disc does not presuppose parasitic or predatory habit as the living non-feeding species use their oral discs to move stones for nesting and to anchor to the stone and the partner female during the mating⁵. Alternatively, we propose that these early lampreys’ well-developed attaching skills might be for hitch-hiking on other delivers, e.g., bony fishes or sharks, to expand their distribution, or for scraping algal mats on other aquatic animals to open up a new niche to avoid the competition of the diversified jawless contemporaries³².

Along the nearly 100-million-year geological interval after the Carboniferous, lampreys had been confronted by similar challenge of the food resource because the thin-scaled fishes (leptolepids plus more advanced teleost fishes) and other potential hosts, e.g., the elasmobranch sharks, were not abundantly emergent until the Early Jurassic^34,35, a timeline congruent with the estimated age of the node encompassing all known lamprey lineages with modern triphasic life history (Fig. 3).

Therefore, provided with increased feeding opportunities and much better-developed feeding structures, lampreys from the Jurassic onward had evolved sufficiently large body size. This novelty, together with the enhanced swimming capability, should have rendered the lampreys elevated hydromechanical advantage and reproductive output to withstand the distance, rigor and mortality of the upstream migration. In effect, these paved the way for lampreys’ habitat expansion to the freshwater system and fueled the innovation of the life history strategy by introducing a radical metamorphic phase.

The early biogeographical history of modern lampreys

Living lampreys’ anti-tropical distribution is effectively restricted in temperate or sub-arctic regions, north and south of the 30° parallel and marked out by the annual 20℃ isotherm⁶. The adaptation to cool or cold waters might also exist in early lampreys. The palaeotemperature curve projected to our dated petromyzontiform timetree (Fig. 4) shows that the emergence of recorded fossil lampreys appears to match the cool or cold geological intervals and came from productive areas influenced by continental ice sheets, cooling events or topographical highland^13,36–39 (Supplementary Materials). This could suggest that lampreys’ ecological preference might have remained static throughout their history and hence being more frequently discovered in cool settings.

The phylogenetic relationships of Mesozoic stem species and crown-group lampreys implies a trans-equatorial dispersal from Northern to Southern Hemispheres sometime after the age of Yanliaomyzon (Fig. 4). Given early lampreys’ occurrences in the Euramerican palaeoequatorial regions in the Late Carboniferous Ice Age^36,37, such a scenario was fairly possible during the cool intervals in the Tithonian-early Barremian Cool Interval and the Aptian-Albian Cold Snap³⁸ when some cold-adapted nannofossil species had dispersed from high-latitude to low-latitude regions⁴⁰. As for lampreys, the increased body size (e.g., Yanliaomyzon occisor) at this evolutionary level must have given them long-distance dispersal capability⁵ and therefore made this voyage more manageable, just like the case of the pouched lamprey Geotria australis now inhabiting both sides of southern Pacific Ocean^27,41, even though bearing a much more shortened dorsal fin and hence lower hydromechanical efficiency than Yanliaomyzon and Mesomyzon. As extant predatory lampreys, e.g., Geotria, may follow the movements of fish shoals over considerable distances⁶ and in varying water depth⁴², the diversification and global distribution of the potential host fishes from the Late Jurassic to Late Cretaceous eras³⁴ could have also promoted the contemporaneous lampreys’ trans-equatorial dispersals.

The formation of modern lampreys’ distribution pattern remains elusive. The southern lampreys were conventionally proposed as the derivatives of Northern Hemispheric lineages via a ‘pre-Tertiary’ departure^1,5,6. With the advent of cladistics and molecular clock, the petromyzontiform crown age was estimated to range from 280-220 Ma²⁴ to 170 Ma²³, hence predating the tectonic splits of the Gondwana³³. Living lampreys’ ‘poles-apart’ distributional pattern was also traditionally attributed to the drift vicariance related with the breakup of Pangea into northern and southern landmasses⁶. Contrary to the past efforts, our study points to the Southern Hemisphere as the biogeographic source for modern lampreys and pushes the petromyzontiform crown and southern-northern divergence to much younger intervals. These ages correspond to two relatively cool intervals with the former marking the ending of the Cenomanian-Turonian Thermal Maximum, which might have wiped out the stem lineages, and the latter culminating immediately in the Palaeocene-Eocene-Thermal-Maximum (PETM)³⁸. The warmed tropical and low-latitude seas and the declined equator-to-pole temperature gradient during PETM ⁴³should have greatly restricted the distribution of these cold-water animals and ultimately shaped their anti-tropical, disjunct biogeographical pattern.

The Northern Hemispheric lampreys were estimated to begin their diversification in the late Oligocene after the earth entered an ‘ice-house’ phase⁴⁴ and Greenland glacial ice and pan-Arctic sea ice first emerged⁴⁵. Notably, this timing is also compatible with the diversification of the major fish and aquatic mammalian hosts of modern lampreys^{44, 46–50}. The favorable climatic settings and increased food supply should have boosted the radiation of lampreys in the Northern Hemisphere, which is also supported by the more numerous and diversified riverine systems in northern temperate regions than in corresponding areas of the Southern Hemisphere^5,11.

adc, anterior tectal cartilage; adf, ‘anterior dorsal fin’ (dorsal fin); af, anal fin fold; ba, branchial apparatus; bp, branchial pouches; ca, cloaca (anus); cot, circumoral teeth; da, dorsal aorta; dcf, dorsal lobe of caudal fin; dt, oral disc teeth; cf, caudal fin; e, eyes; dt, detritus; go, external gill openings; gp, gular pouch; ic, intestine contents; io, infraoral lamina; ll, longitudinal lingual lamina; ll.l, left longitudinal lingual lamina; ll.r, right longitudinal lingual lamina; lv, liver; ns, olfactory organ ; oc, otic capsule; od, oral disc; of, oral fimbriae; op, oral papillae; paf, preanal skin fold; pc, pericardial cartilage; pdc, posterior dorsal cartilage; pdf, ‘posterior dorsal fin’ (anterior part of caudal fin); pt, piston cartilage; so, supraoral lamina; tl, transverse lingual lamina; vcf, ventral lobe of caudal fin; vl, velum; V1?, ophthalmic ramus of trigeminal nerve?.

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Competing interests.

The authors declare no competing interests.

Funding:

National Natural Science Foundation of China (42288201 to Z. H. Zhou); Strategic Priority Research Program of CAS (XDB26030304; XDA20070203); Hundred Young Talents Program of Chinese Academy of Sciences (CAS) to C. Zhang; Chinese Academy of Sciences President’s International Fellowship for Distinguished Scientists to P. Janvier (2019DB0022).

Author contributions:

F.X.W. designed this study, prepared figures, and wrote manuscript; P.J. contributed to drafting manuscript; C.Z. performed analyses, prepared figures, and drafted manuscript, especially the method section.

Acknowledgments.

We thank the organizers of Second Tibetan Plateau Scientific Expedition (STEP) for financial and logistic support during the field work and data collection. We thank M.-M. Chang for enlightening discussions; Special thanks go to X. L. Wang for specimen collection; Thanks to D. S. Miao for stylistic improvement of the abstract of the manuscript. We appreciate the help of H. B. Wang and Z. Q. Yu during the fieldwork and Y. M. Hou, C. Zhang for producing computed tomography and W. Gao and Z. Feng for photographing; Y. F. Chen for fossil preparation. We thank Q. M. Qu, D. Y. Huang, Y. A. Zhu and T. Miyashita for helpful discussions, L. P. Dong, C. C. Liao, Q. G. Jiangzuo for providing some literatures, H. Li for assisting in data collecting and G. H. Xu for helping with photographing.

There is NO Competing Interest.

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Lampreys underwent radical changes in ecology and morphology during the Jurassic era

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