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The fate of mammals after the extinction of dinosaurs

Researchers describe the dynamics of mammal diversification after the mass extinction at the end of the Cretaceous

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When talking about mass extinction, it is common to imagine a meteor falling to Earth and decimating dinosaurs, but that is not the case. The various mass extinctions in the history of the planet have occurred differently among groups of living beings. One example is mammals, a class of vertebrates that already existed at the time of the dinosaurs and survived the massive extinction event 66 million years ago, which marked the end of the Cretaceous period.

There were four lineages of mammals contemporary with the giant reptiles. They all survived. Some came out more scorched, others less. In a study published in BiologyLetters, biologists Tiago Bosisio Quental, from the University of São Paulo, and Mathias Pires, from Unicamp, seek to understand how different groups of mammals went through mass extinction at the end of the Cretaceous. The work included support from FAPESP.

"When we talk about mass extinctions, we imply an event of large proportions, during which a large number of species became extinct in a relatively short period," said Pires.

Another way to look at mass extinctions is to look at the number of species in the fossil record. It appears that in a given geological period a mass extinction occurred when the total number of species that disappeared from the fossil record is much higher than the number of new species.

"In other words, it is when the rate of extinctions, the speed at which species are lost, exceeds the rate of speciation, the speed at which species are generated. This makes the diversification rate negative, which is given by the difference between the two rates ", said Pires.

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In the image: origination, extinction and diversification rates for the three clades [groups with a common ancestor] of mammals in North America. Dotted lines denote the Cretaceous-Paleogene boundary / Biology Letters)

In the fossil record of the last 500 million years, five major mass extinctions (and many others on a smaller scale) have been identified. They occurred for a variety of reasons, such as magmatic leaks over hundreds of thousands or millions of years, releasing billions of tons of greenhouse gases that poisoned the atmosphere and blocked solar radiation.

This is what happened in the worst of the mass extinctions, 252 million years ago, which marked the transition from the Permian to the Triassic periods (and from the Paleozoic to the Mesozoic eras), when more than 90% of species disappeared. Mass extinctions also occurred when there was a massive release of billions of tons of carbon dioxide (CO2) trapped in the oceanic subsoil, causing a mega-greenhouse effect – as is speculated to have occurred at the end of the Triassic period, 201 million years ago, with the loss of 80% of species.

Or the opposite, with the sequestration of billions of tons of CO2 of the atmosphere, which dropped temperatures, causing severe planetary glaciation. It was like this 444 million years ago, at the end of the Ordovician period, when 86% of life forms disappeared.


K-Pg Event

The mass extinction 66 million years ago is called the K-Pg event, an acronym that refers to the moment in which the Cretaceous period (Kreide, in German) ends and the next period, the Paleogene (Pg), begins. On a broader time scale, the K-Pg event was the geological instant that marks the end of the Mesozoic era, the one dominated by dinosaurs, and the beginning of the Cenozoic, the last 66 million years.

The K-Pg event was caused by the association of two factors: devastating magmatic leaks in what is now India, combined with the collision of a celestial body 10 kilometers in diameter on the Yucatán peninsula, in present-day Mexico.

"All these episodes of mass extinction are heterogeneous. They had different causes and occurred in different ways. Likewise, their impact on life forms was not absolute, but relative. Some groups suffered more, others less. Some disappeared, while others took advantage of the new post-catastrophe environmental conditions to quickly diversify", said Pires.

In the new work, the researchers sought to understand how the different mammal lineages that existed at the end of the Cretaceous overcame the biotic bottleneck of the K-Pg event. Daniele Silvestro, from the University of Gothenburg (Sweden), and Brian Rankin, from the University of California at Berkeley (United States), also participated in the study.

The large class of mammals emerged in the Triassic at least 220 million years ago, the age of the oldest known fossil. At the end of the Cretaceous, the lineage was quite diverse. There were placentals (as eutherians are popularly known), a lineage to which the Homo sapiens, as well as all primates, rodents, bats, cetaceans and ungulates, among others.

There were also marsupials (or metatherians), a group that today houses possums, kangaroos and koalas. They shared the scene with the group of monotremes and, finally, with the multituberculates (their name derives from the specific shape of their teeth, with several tubercles).

The new study highlights that the Cretaceous mass extinction hit mammals hard. This does not mean that all four groups suffered with the same intensity. Mass extinction was more severe for some than others.

During the Cretaceous, between 145 and 66 million years ago, multituberculates were the dominant and most diverse lineage among mammals. This is known because, in the fossil record that precedes the K-Pg event, multituberculate fossils are the vast majority. Placental and marsupial fossils, although less numerous, are also found in good numbers.

The exception is monotremes. As is the case today, when there are only two families of living monotremes – which include the platypus and the echidna –, the fossil record of monotremes is very rare, both before and after the Cretaceous, suggesting that this group has always been relatively marginal in relation to other mammalian lineages. It is also for this reason that this lineage was not included in the study.

Knowing that there were multituberculates, placentals and marsupials, which group of mammals was most severely affected in K-Pg? From which lineage did the most genera survive? Which group showed the greatest increase in diversity (greatest speciation) in the millions of years immediately following the biotic bottleneck? Which group never recovered from the cataclysm?

The only way to try to obtain answers to these questions is to resort to the fossil record found in the same region of the planet, in order to try to guarantee that, 66 million years ago and in that region, the catastrophe struck in a more or less equivalent way on all groups of mammals.

Quental and Pires chose North America as the study site, since 150 years of continuous paleontological prospecting on that continent provides a rich panel of mammal diversity before, during and after the K-Pg event.

"North America presents a fossil record of sufficient quality for this type of study. Other studies have already been carried out analyzing how mammals overcame the Cretaceous extinction, but as far as we can see this is one of the first to analyze the dynamics of the diversification of distinct lineages of mammals,” said Quental.

The scientists used a data set with 188 recent fossil assemblages from the Cretaceous and Paleocene – covering a time span from 69,9 million years to 55 million years ago – formations located in the western interior of North America.

"The North American mammal fossil record has very well-studied assemblages with dates around the K-Pg event, with fossil occurrences being relatively well resolved, minimizing taxonomic uncertainty. The dataset we used includes information on almost 290 mammalian genera, including multituberculates, eutherians and metatherians”, said Quental.

Several advanced statistical methods were used to identify patterns of origination, extinction and diversification before, during and after the K-Pg. The results showed that the three lineages went through the mass extinction in very different ways.

The study indicates that the origination rate of Methateria (marsupials), for example, remained approximately constant throughout the time interval studied. However, a clear extinction peak is identified during K-Pg, generating a negative net diversification balance. After the K-Pg event, the extinction rate gradually decreased. However, net negative diversification persisted for more than 2 million years, until about 64 million years ago.

As for multituberculates, they were diversifying at the end of the Cretaceous, showing high rates of origination and relatively low rates of extinction. Around the K-Pg limit, the extinction rate remained low, but drops in the origination rate were observed, which dropped the diversification of multituberculates to close to zero. In other words, during the K-Pg the rate of diversification is in balance, as approximately the same number of multituberculate genera are originating and becoming extinct.

According to the study, after the K-Pg, although the extinction rate of multituberculates continued to fall, the decline in the origination rate was even greater, consequently leading to negative diversification. In other words, the number of multituberculate genera continued to decrease during the remainder of the period analyzed, until 55 million years ago. This decline appears to have persisted for much longer, given that multituberculates progressively disappeared from the world's fossil record, until, finally, the lineage ended about 35 million years ago.

It is speculated that the reason for the end of the multituberculates would have been the increasing competition with a new lineage of eutherians, the rodents, whose order originated shortly after the K-Pg event, already in the Paleogene period.

As for eutherians (placentals), the study shows high origination and high extinction near the K-Pg limit, resulting in an inflection in diversity. Origination rates were much higher than those of extinctions, except for the period between 66 million years ago and 64 million years ago.

Soon after, there is a second pulse of origination, accompanied by a drop in extinction rates, a sign of the occurrence of a short burst in diversification. Around 62 million years ago, the origination of eutherians decreases, while diversification remains around zero, suggesting a balance of diversity.

"We found three patterns of diversification among mammal groups. Metatheria behaves in the classic way in a mass extinction. Several extinctions cluster together in time, leading to a severe drop in diversification,” said Quental.

According to the researcher, in multituberculates the decrease in diversification and the subsequent loss of diversity were driven by the decline in origination rates and not by extinction, that is, they lost diversity because they took a long time to generate new species.

"Eutherians, on the other hand, show a more complex dynamic of rise and fall, more precisely attributed to rapid oscillations in the speciation rate during and shortly after the K-Pg, at the same time that the extinction rate increases, but not so much that cause negative diversification for a long time," Quental said.

Pires highlights that the study shows that the mass extinction of K-Pg was ecologically selective among mammalian lineages, “with a concentration of extinctions between specialized carnivorous metatherians and insectivorous eutherians, while the more generalist eutherians and multituberculates maintained greater diversity” .

Although the results indicate that eutherians (placentals) suffered substantial losses in the K-Pg threshold, these losses were offset by increased origination. Diversification may have occurred among the surviving eutherians, thanks to the arrival in North America of other groups of eutherians from other continents.

"The plasticity of multituberculate diets may have allowed the groups to persist, explaining the low extinction rates. The ecological and taxonomic diversity of multituberculates was increasing during the late Cretaceous. However, our analyzes show that multituberculates did not compensate for the losses by extinction, as they generated less and less diversity, unlike eutherians, whose losses were compensated by high origination rates”, said Pires.

The researchers' conclusion indicates that, when clades (groups with a common ancestor) are evaluated individually, mass extinction events can be seen as changes in extinction, origination or both regimes.

“This means that studies on macroevolutionary phenomena that are focused on large taxonomic groups may be failing to tell a much richer macroevolutionary story, only perceived at more subtle taxonomic scales”, they highlight.

The article

The article Diversification dynamics of mammalian clades during the K–Pg mass extinction (doi: 10.1098/rsbl.2018.0458), by Mathias M. Pires, Brian D. Rankin, Daniele Silvestro and Tiago B. Quental, can be read at http://rsbl.royalsocietypublishing.org/content/14/9/20180458

 

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