Artist’s impression of Dryolestes on a stegosaur tail spike.
New technology has enabled a team of scientists to examine in microscopic detail, the growth rings in the root cement of the fossilised teeth of early mammals, and to make a surprising discovery - the earliest mammals lived considerably longer than equivalent-sized mammals do today, but they took longer to reach sexual maturity.
These growth rings are like those of trees and record the annual growth of the mammal. They can be seen using a technique called synchrotron X-ray tomography in which electrons are accelerated to near light-speed. This means that like x-rays they can penetrate solid objects such as fossils and bone, which do not need to be cut into thin slices, and like an electron microscope, because electrons have such short wave-lengths, they can resolve much finer structures, hence these microscopic growth rings become visible.
Tell me about the early mammals and proto-mammals of the Early to Late Jurassic, please. The Early to Late Jurassic period (about 201 to 145 million years ago) was a time of significant evolutionary change, particularly for early mammals and their precursors, known as proto-mammals. During this time, mammals were not yet dominant on Earth, but their ancestors were evolving key traits that would later define the class Mammalia.The discovery by an international team of scientists led by Dr. Elis Newham, now at Queen Mary University of London, who during the study, was an Alexander von Humboldt Research Fellow at the University of Bonn, is the subject of an open access paper in Science Advances and is explained in a brief news item from the Rheinische Friedrich-Wilhelms-Universität Bonn:
Proto-Mammals (Synapsids)
The story of early mammals begins with their distant ancestors, the synapsids. These were a group of amniotes that included the ancestors of mammals. By the Jurassic period, most of the synapsid lineages that resembled reptiles had already gone extinct, but a particular group, the Therapsids, had given rise to more mammal-like forms.
Early Mammals
- Cynodonts:
- Cynodonts are a subgroup of therapsids that are particularly important in the evolution of mammals. By the Jurassic period, many cynodonts had evolved features that were very mammal-like, including differentiated teeth (incisors, canines, and molars), a more efficient jaw joint, and a secondary palate that allowed them to breathe while chewing.
- Notable Jurassic cynodonts include Tritylodonts and Tritylodontids, which were herbivorous and possessed complex teeth for processing plant material.
By the Jurassic, the earliest true mammals had already evolved from cynodont ancestors. These early mammals were small, nocturnal creatures that filled ecological niches left by the dominant reptiles of the time, including the dinosaurs.
- Morganucodontids:
- These are among the earliest known true mammals, dating from the Late Triassic to the Early Jurassic. Morganucodon is a well-known example. It was a small, shrew-like animal that had a double-jointed jaw, an intermediate feature between cynodonts and modern mammals.
- Morganucodontids had a mixed diet of insects and small invertebrates, and they likely lived in burrows.
- Docodonts:
- Another group of early mammals from the Jurassic, the Docodonts, were small, with complex teeth adapted for an omnivorous diet. A famous member of this group is Docodon.
- Docodonts had a more developed jaw structure and ear bones, showing further evolution towards the modern mammalian condition.
- Eutriconodonts:
- These mammals, like Eomaia and Repenomamus, were slightly more advanced and are sometimes considered closer to modern placental mammals. They had three-cusped teeth, which is a typical mammalian characteristic.
- Some eutriconodonts were relatively large for the time, with Repenomamus being one of the largest, capable of preying on small dinosaurs.
- Multituberculates:
- A highly successful and long-lived group of early mammals, Multituberculates had rodent-like teeth and were among the first mammals to specialize in herbivory. They survived well into the Cenozoic era.
- They are known for their multi-cusped teeth, which were well-suited for grinding plant material.
- Haramiyidans:
- These small mammals, with teeth adapted for a herbivorous diet, are known from both the Triassic and Jurassic periods. Haramiyavia is an example from this group.
- Haramiyidans are a bit enigmatic, with some debate over their exact placement in the mammal evolutionary tree. Some consider them closely related to Multituberculates.
Evolutionary Significance
During the Jurassic, these early mammals and their proto-mammalian ancestors were laying the groundwork for the traits that would later allow mammals to thrive. They were typically small, nocturnal, and occupied ecological niches that allowed them to coexist with the dominant dinosaurs. Their evolution included the development of endothermy (warm-bloodedness), hair, and more complex brain structures, all of which were crucial for their survival and diversification.
In summary, the Jurassic period was a critical time in mammalian evolution, marking the transition from reptile-like synapsids to the first true mammals. Although overshadowed by the dinosaurs, these early mammals were evolving the traits that would eventually lead to their dominance after the extinction of the dinosaurs at the end of the Cretaceous period.
Early Mammals Lived Longer
University of Bonn researchers are studying the lifespan and growth patterns of early mammals
What distinguishes the growth and development patterns of early mammals of the Jurassic period? This is the question jointly investigated by researchers of Queen Mary University of London and the University of Bonn. Paleontologists have been able to gauge the lifespan and growth rates of these ancient animals, and even when they reached sexual maturity, by studying growth rings in fossilized tooth roots. The study has now been published in the journal Science Advances.
Never before have we been able to reconstruct the growth patterns of these early mammals in such detail.
Dr. Elis Newham, lead author.
School of Engineering and Materials Sciences
Queen Mary University of London, London, UK.
For the study, the team analyzed fossilized tooth roots of mammal species from the Early to Late Jurassic periods (200-150 million years ago) found at three separate sites. The finds made in Wales are of some of the oldest known mammalian precursors from the Early Jurassic period, while the fossils found in Oxfordshire, UK are of a very broad array of coexisting early mammals. The fossils from the third site in Portugal date from the Late Jurassic.
Fossil tooth roots X-rayed
The research team studied the fossils using a technique called synchrotron X-ray tomography in which electrons are accelerated to near light speed (unlike regular X-ray imaging). The technique affords several advantages, starting with the fact that the fossils no longer have to be prepared, i.e. cut up into slices, so they can be analyzed whole. Furthermore, images obtained via synchrotron X-ray tomography are of higher quality than images from conventional X-ray microtomography.
Researchers were able to image tiny growth rings in fossilized root cement—the bone tissue that attaches the teeth to the jaw.
The rings are similar to those in trees, but on a microscopic level. Counting the rings and analyzing their thickness and texture enabled us to reconstruct the growth patterns and lifespans of these extinct animals.
Professor Thomas Martin, senior author
Section Palaeontology
Bonn Institute of Organismic Biology
Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany.
The researchers determined that the first signs of the growth patterns characteristic of modern mammals, such as a puberty growth spurt, started emerging roughly 150 million years ago. Early mammals grew much more slowly but lived substantially longer than today’s small mammals, with lifespans of eight to fourteen years instead of just one or two as in modern mice, for example. However, it took early mammals years to reach sexual maturity, again in contrast to their modern descendants which reach sexual maturity in just a few months.
Our findings suggest that the distinctive life history patterns of mammals, characterized by high metabolic rates and extended parental care phases for example, have evolved over millions of years The Jurassic period appears to have been a crucial time for this shift.
Dr. Elis Newham.
Fossil jaw of an early mammal - with complete tooth row, prepared for scanning in the synchrotron.© Photo: Elis Newham.
Publication:
AbstractWhat's very clear in this paper is not just the authors' acceptance of the Theory of Evolution as the best explanation for the observation, but the way their findings inadvertently refute creationism, not just by the time-frame involved (hundreds of millions of years, not just a few thousand years) but the illustration of something that is often a feature of evolution, but not something that would be a feature of intelligently designed systems by an omniscient designer - the evolutionary trade-off. There was a trade-off between an earlier strategy - slow sexual maturity and a relatively long reproductive life, and the later rapid maturity and a shorter reproductive life.
We use synchrotron x-ray tomography of annual growth increments in the dental cementum of mammaliaforms (stem and crown fossil mammals) from three faunas across the Jurassic to map the origin of patterns of mammalian growth patterns, which are intrinsically related to mammalian endothermy. Although all fossils studied exhibited slower growth rates, longer life spans, and delayed sexual maturity relative to comparably sized extant mammals, the earliest crown mammals developed significantly faster growth rates in early life that reduced at sexual maturity, compared to stem mammaliaforms. Estimation of basal metabolic rates (BMRs) suggests that some fossil crown mammals had BMRs approaching the lowest rates of extant mammals. We suggest that mammalian growth patterns first evolved during their mid-Jurassic adaptive radiation, although growth remained slower than in extant mammals.
INTRODUCTION
The physiological maintenance of consistent body temperatures above ambient levels in mammals results in basal metabolic rates (BMRs) higher than equivalent resting metabolic rates in ectothermic reptiles and amphibians (1–9). High BMRs allow for rapid skeletal growth in juveniles that slows with the attainment of sexual maturity [which generally occurs significantly earlier than in ectothermic vertebrates (10–15)]. This creates sigmoidal growth rate patterns through life (Figs. 1 and 2) in each of the three major extant mammalian clades: Placentalia (16), Marsupialia (2, 16), and Monotremata (13). Often classed as “determinate” growth patterns, the mammal (and avian) condition broadly differs from determinate growth patterns in other extant vertebrates (e.g., lepidosaurs) due to the steeper truncation from exceptionally rapid juvenile growth rates to minimal adult growth over a relatively short period of time. The BMR remains elevated in sexually mature mammals, which is believed to limit the maximum life span of mammals compared to ectotherms of similar size and ecology due to increased rates of metabolic oxidative stress (6, 9). Understanding how this characteristic suite of life history parameters—life span, growth rates, and growth patterns—developed through the fossil record is critical for our understanding of mammalian physiological evolution.
Numerous studies have sought to identify growth patterns in fossil mammals and their synapsid relatives (17–21), concluding that mammaliaforms (stem lineage mammals) may have retained labile growth patterns and slow juvenile growth rates (relative to extant mammals) through the Mesozoic (18). Conflicting conclusions, from mandibular size and links with the origin of diphyodonty (a single replacement of teeth, autapomorphic to Mammaliaformes; Materials and Methods) (4, 19, 21), have been used to suggest that mammalian determinate growth (earlier and steeper truncation in growth rates) evolved on the mammalian stem lineage. However, these interpretations have lacked the crucial aspect of a time frame, i.e., life span. Without evidence of the individual age of the specimens studied, the reported growth changes cannot be calibrated over the life span of the respective taxa, and it is not feasible to estimate the true growth rates. This undermines the ability to accurately distinguish growth patterns and compare them to those of extant mammals.
Fig. 1. Comparison between cementum growth in nonmammalian mammaliaforms, early mammals, and extant mammals.
(A to C) Details of the cementum (highlighted) of (A) docodontan Krusatodon NHMUK PV M36541, (B) cladotherian Dryolestes Gui Mam 1191, and (C) primate M. mulatta k39. (D to F) Straightened sections from (A) to (C), respectively, including the external-most dentine hyaline layer of Hopewell-Smith (light phase indicated by orange arrows) used for measuring cementum increment widths along eight evenly spaced radial transects (yellow bars for examples) between the inner cementum boundary/cementum-dentine junction (pink asterisks) and outer cementum boundary/root surface (green asterisks). (G to I) Mean grayscale values (SRCT data) measured across 10-pixel-thick transects in (D) to (F), respectively; light increments forming peaks, and dark increments forming troughs. Annual growth measured as the spacing between light increments (Materials and Methods) (fig. S1). Schematic patterns for spacing/growth rate through life represented in the right-hand summary charts. (J to L) 3D surface plots of grayscale texture in (D) to (F), with differences between known [for (L)] and estimated [for (K)] juvenile versus adult cementum texture highlighted using black dashed-dotted lines (see fig. S1). Black dashed-dotted line in (J) represents periods of life subsampled to test for differences in juvenile versus adult cementum in mammaliaforms. All silhouettes obtained from PhyloPic (http://phylopic.org/) under a public domain license.
Fig. 2. msGRs through life measured for fossil mammaliaforms and selected extant mammals. (A) Time-calibrated phylogeny with major groups, sample number, and origin highlighted. (B) msGR curves for nonmammalian mammaliaforms, fossil mammals, and selected extant mammals. Data restricted to years of life represented by ≥3 specimens (for full life-span estimates, see Fig. 3). Dashed portions of extant plots represent the mean period for attainment of sexual maturity for the respective taxon. Bracketed vertical lines represent SDs for subsampled measurements (Materials and Methods). Symbols (see legends) represent mean msGRs for the respective taxon during the respective year of life. Lines for all taxa represent best-fitting nonlinear models (Table 1). Dashed-dotted portions of fossil crown mammal plots represent estimated periods for attainment of sexual maturity. Extant mammals included were chosen due to their comparable sampled life spans and body masses to fossil mammaliaforms and phylogenetic diversity; see fig. S5 for full extant sample. Source data are provided as data S1. Time-calibrated Mesozoic mammaliaform phylogeny sourced from Araújo et al. (8). Extant mammal phylogeny sourced from Vertlife (http://vertlife.org/). All silhouettes obtained from PhyloPic (http://phylopic.org/) under a public domain
This limit was recently overcome through the application of cementochronology, using synchrotron radiation–based x-ray computed tomography (SRCT) (4). Dental cementum, the mineralized tissue surrounding tooth roots and connecting them to the periodontal ligament, is unique among mammalian hard tissues as its growth is continuous throughout life and it is not remodeled and rarely resorbed, and annual increments can be counted (22, 23) (Fig. 1). Here, we demonstrate how counting cementum growth layer groups (Figs. 1 and 2) and analyzing their radial thickness and texture (fig. S1) can serve as a surrogate measure for mammal life span, growth rate, and growth pattern. A critical time in the evolution of these life history parameters was across the Jurassic mammalian adaptive radiation (24, 25), and so we examine fossilized cementum increments in stem and crown lineage mammals from three localities, each within either the Early, Middle, or Late Jurassic. This has provided an unparalleled opportunity to study samples that span the mid-Jurassic radiation both phylogenetically and temporally, in quantities sufficient for the population-level sampling necessary to characterize life history.
Cementochronology of Mesozoic mammaliaforms
Cementochronology is an important tool to investigate life history (26–32). Nondestructive SRCT imaging allows counting of annual growth layer groups [a pair of one thick “light,” higher density increment deposited during favorable seasons and one thin “dark,” lower density increment deposited during unfavorable seasons (26, 27)] deposited for each year of life in the acellular extrinsic fiber portion of the cementum tissue (AEFC) (Materials and Methods) (Fig. 1). Validation studies performed on a wide range of extant (22, 26) mammals of known age suggest that this tissue comprises increments with strong circum-annual periodicity (23), and herein is the tissue referenced when using the term “cementum” (see Materials and Methods for validation of annual periodicity using dentary bone lines of arrested growth in fossil mammaliaforms).
The first application of cementochronology to study the physiological evolution of Mesozoic mammals used SRCT in population-sized samples of the Early Jurassic nonmammalian mammaliaforms Morganucodon and Kuehneotherium (4). This revealed unexpectedly long life spans for their body mass and reptile-like physiology. Both life span and BMR covary with body mass among extant mammals, with larger taxa having lower mass-specific BMRs (msBMRs) and longer life spans (4–6, 9) [although this relationship is complicated among flying/gliding and marine taxa due to their specific ecological requirements; see correspondence between Meiri and Levin (5) and Newham et al. (4, 6)].
Here, we demonstrate how not only counts for life span (Figs. 1 and 2) but also further analysis of the radial thickness and texture (fig. S1) of cementum growth layer groups can serve as a surrogate measure for growth rate and growth pattern. Cementum helps to keep tooth crowns level above the gumline through life as the jaw remodels through growth and crowns are worn from occlusion (22, 26). This is reflected in frequent observations of changes in increment width and quality at the reduction of somatic growth and attainment of sexual maturity in extant mammals (22, 27–32). A number of extant mammal species display a negative sigmoidal trend in cementum increment thickness that follows their somatic growth patterns: rapid juvenile growth is represented by widely spaced irregularly organized increments (28), and the advent of sexual maturity and cessation of somatic growth lead to narrowly spaced, more uniformly organized increments (Figs. 1 and 2) (22, 27–31).
To study the evolution of these life history parameters across the Jurassic mammalian adaptive radiation (24, 25), we analyze the cementum of diphyodont fossil mammaliaforms from three localities that originate between the Early-to-Late Jurassic. The Early Jurassic (Hettangian) Hirmeriella fissure suite (Wales, United Kingdom) includes some of the earliest known nonmammalian mammaliaforms (33); the Middle Jurassic Forest Marble fauna (Bathonian) of Oxfordshire (United Kingdom) includes one of the most taxonomically diverse known faunas of cohabiting nonmammalian mammaliaforms (docodontans) and early theriimorph mammals (34) (therians and all extinct taxa more closely related to therians than to monotremes); and the Kimmeridgian Guimarota fauna (Portugal) provides the most numerous Late Jurassic fossils of nonmammalian mammaliaforms and theriiform mammals currently known (35) (Fig. 2; see Materials and Methods).
We present a method for quantifying growth rates of cementum growth layer groups in volumetric SRCT datasets by counting and measuring distances (in micrometers) between peaks in grayscale values (representative of light circum-annual cementum increments) along radial transects through the cementum in preprocessed and subsampled SRCT slices (Fig. 1; Materials and Methods) (27, 36). Counts are used to estimate life spans (years) (fig. S1) and msBMRs (ml \(\small \ce{O2}\) hour-1 g-1) following the method outlined by Newham et al. (4) (fig. S2). To allow comparison of growth rates between fossil and extant clades of varying body mass, mean width measurements for each year of life were processed to create mass-specific annual growth rates (msGRs; μm year g−1). This was performed using a mass-specific growth ratio created by exponential phylogenetically informed least-squares (PGLS) regression (37) between log-transformed body mass (in grams) and log-transformed width of the first cementum growth layer group (in micrometers) in a sample of 23 extant therian mammals (fig. S3).
[…]
DISCUSSION
Jurassic mammaliaforms on the physiological spectrum
Our results add crucial detail to the evolution of life history across the Jurassic mammalian adaptive radiation. Although our cementum analysis methods are currently limited in use to diphyodont mammaliaform taxa and so conclusions bound to evolution within Mammaliaformes, an evolutionary transition of physiology to a more “mammalian” life history among Middle Jurassic theriiform mammals (fig. S6) supports a delayed acquisition of fully modern mammalian physiological traits suggested by other recent studies (1, 4, 8, 11, 39). Many traits related to endothermy appeared before the mid-Jurassic, but only consistently reached values approaching or within the range of extant mammals during this time. For example, it has been evidenced from long bone histology that longevity and age at sexual maturity both decreased in nonmammaliaform therapsid clades that survived the end-Permian mass extinction (40, 41), with maximum estimated longevity (and so also inferred age at sexual maturity) falling to within 2 years in the earliest Triassic species of Lystrosaurus (41). Botha-Brink et al. (41) showed that both traits returned to values more comparable with those of pre-extinction taxa in clades radiating further into the Triassic. Also, while recent proxy data suggest that body temperatures in several lineages of nonmammalian mammaliaforms may have approached endothermic levels (8), they did not fall consistently within the extant mammalian range until the radiation of crown mammals. Although body temperature evolution has remained uncoupled from BMR evolution across the mammalian phylogeny (7), this is consistent with our predicted BMRs and evolutionary patterns in encephalization quotients (relative brain size) (42).
Determinate growth patterns themselves are not exclusively related to endothermy (3, 43). However, the pattern of determinate growth combined with elevated juvenile growth rates shown here for extant mammal cementum and elsewhere for skeletal (44) and bodily growth (10) is indicative of their elevated, endothermic BMR values. This supports the hypothesis that Jurassic mammals had not developed life histories similar to extant terrestrial mammals of comparable body mass; comparatively rapid juvenile growth rates (fig. S5), sexual and skeletal maturity before 2 years of age (Fig. 3C), and maximum wild life spans of 7 years or less [aside from long-lived and secondarily dwarfed Microcebus primates (45)] (Fig. 3A).
The dynamics of this trade-off may have been related to the evolution of warm-bloodedness in the true mammals, so these nonmammalian mammaliaforms represent a transitional stage between the cold-blooded ancestor of mammals and warm-blooded mammals a transition that continued as modern mammals evolved from the first true mammals. With intelligently designed species there would be no record of transition, no need for evolutionary trade-offs and compromises, and no earlier, less efficient reproductive strategies.
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