Causes of global extinctions in the history of life: facts and hypotheses (2024)

Language: English | Russian

Abstract

Paleontologists define global extinctions on Earth as a loss of about three-quarters of plant and animalspecies over a relatively short period of time. At least five global extinctions are documented in the Phanerozoicfossil record (~500-million-year period): ~65, 200, 260, 380, and 440 million years ago. In addition, there isevidence of global extinctions in earlier periods of life on Earth – during the Late Cambrian (~500 million yearsago) and Ediacaran periods (more than 540 million years ago). There is still no common opinion on the causesof their occurrence. The current study is a systematized review of the data on recorded extinctions of complexlife forms on Earth from the moment of their occurrence during the Ediacaran period to the modern period. Thereview discusses possible causes for mass extinctions in the light of the influence of abiogenic factors, planetaryor astronomical, and the consequences of their actions. We evaluate the pros and cons of the hypothesis onthe presence of periodicity in the extinction of Phanerozoic marine biota. Strong evidence that allows us tohypothesize that additional mechanisms associated with various internal biotic factors are responsible for theemergence of extinctions in the evolution of complex life forms is discussed. Developing the idea of the internalcauses of periodicity and discontinuity in evolution, we propose our own original hypothesis, according to whichthe bistability phenomenon underlies the complex dynamics of the biota development, which is manifested inthe form of global extinctions. The bistability phenomenonarises only in ecosystems with predominant sexualreproduction. Our hypothesis suggests that even in the absence of global abiotic catastrophes, extinctions ofbiota would occur anyway. However, our hypothesis does not exclude the possibility that in different periods ofthe Earth’s history the biota was subjected to powerful external influences that had a significant impact on itsfurther development, which is reflected in the Earth’s fossil record.

Keywords: Earth’s fossil record, evolution of global ecosystems, mass extinctions, dynamic systems, complex dynamics, periodicity, modeling

Abstract

Палеонтологи характеризуют глобальные вымирания на Земле как потерю ~3/4 существую-щего биоразнообразия на большей части земного шара за относительно короткий геологический про-межуток времени. В палеонтологической летописи Земли, описывающей период фанерозоя (~500 млнлет), документировано как минимум пять таких глобальных вымираний: ~65, 200, 260, 380 и 440 млн летназад. Существуют данные о возможности глобальных вымираний в более отдаленные периоды жизни наЗемле – в позднем кембрии (~500 млн лет назад) и эдиакарии (более 540 млн лет назад). Общего мненияо причинах их возникновения до сих пор не сформировано. В настоящем обзоре систематизированы до-кументированные факты глобальных вымираний сложных форм жизни на Земле с момента их возникно-вения в эдиакарии и до современного периода. Рассматриваются возможные причины их возникновенияс точки зрения воздействия абиогенных факторов, планетарных или астрономических, и последствий ихдействия. Анализируются данные «за» и «против» гипотезы периодичности массовых вымираний био-разнообразия морской биоты в фанерозойский период. Обсуждаются факты, позволяющие высказыватьгипотезы о наличии дополнительных механизмов возникновения кризисов в эволюции сложных формжизни на Земле, связанных с различными внутренними биотическими факторами. Развивая тему внутрен-них причин периодичности и прерывистости эволюционного процесса, мы высказываем собственную,оригинальную гипотезу, согласно которой глобальные вымирания являются отражением сложной динамики изменения уровня биоразнообразия на Земле и следствием феномена бистабильности. Этот фено-мен возникает только в экосистеме, бóльшая часть организмов которой размножается половым путем.Данная гипотеза говорит о том, что, если бы даже не было никаких глобальных катастроф абиотическо-го характера, кризисы в развитии биоты возникали бы все равно. Однако гипотеза не исключает, что вопределенные моменты времени биота Земли подвергалась мощным внешним воздействиям, оказавшимсущественное влияние на ее дальнейшее развитие, что нашло отражение в конкретных палеонтологиче-ских данных.

Keywords: палеонтологическая летопись Земли, эволюция глобальных экосистем, массовые вымирания, динамические системы, сложная динамика, периодичность, моделирование

Introduction

Global extinctions on Earth are defined by paleontologists asa loss of about three-quarters of the existing biodiversity in arelatively short interval of geologic time. At least five globalextinctions are documented in the Phanerozoic fossil record(~500 million years). These are the Cretaceous-Paleogeneextinction event (~65 million years ago), the Triassic-Jurassicextinction event (~200 million years ago), extinction near thePermian-Triassic boundary (~260 million years ago), the lateDevonian extinction (~380 million years ago), and extinctionnear the Ordovician-Silurian boundary (~440 millionyears ago). These five extinction events were first describedas “Big Five” extinctions based on the analysis of more than36 thousand kinds of marine invertebrate fossils, which werecatalogued in the D.M. Raup and J.J. Sepkoski’s database(Raup, Sepkoski, 1982). Some researchers argue that a sixthmass extinction is currently underway on our planet. Thisopinion is based on the estimates of species extinction ratesin the current period, which were found to be comparable tothose during global extinctions estimated on the basis of paleontologicaldata (Barnosky et al., 2011; Ceballos et al., 2015).

In the last decade, intensive analysis of fossil material hasrevealed new examples of mass extinctions of complex lifeforms on Earth. There is evidence that during the early periodsof life on Earth – in the Late Cambrian (~500 million yearsago) and during the Ediacaran period (> 540 million yearsago) (Gill et al., 2011; Darroch et al., 2015), extinctions wereglobal. Extinction during the Ediacaran period is consideredto be the first mass extinction of complex life forms on Earth(Darroch et al., 2015). Let us consider the facts and hypothesesconcerning the causes of global extinctions.

Mass extinctions as a resultof global disasters of an abiotic nature

A number of abiogenic factors has been described that couldpotentially cause most of the big extinctions detected in theEarth’s fossil record. This does not apply to the biodiversityloss during the late Ediacaran period (Xiao, Laflamme, 2009;Buatois et al., 2014; Darroch et al., 2015), the late Cambrianperiod (Gill et al., 2011), and the modern period (Barnoskyet al., 2011; Ceballos et al., 2015).

The most well-known abiogenic factors that have been associatedwith the environmental disasters are: the struck of amassive asteroid ~65 million years ago (Alvarez et al., 1980,1981; Schulte et al., 2010; Kaiho, Oshima, 2017), volcanicactivity and global warming ~200 million years ago (Marzoliet al., 1999; Whiteside et al., 2010; Blackburn et al., 2013;Thibodeau et al., 2016; Miller et al., 2017; Percival et al., 2017; Heimdal et al., 2018), trappean eruptions ~260 millionyears ago (Huey, Ward, 2005; Wignall et al., 2009; Rampinoet al., 2017), as well as the major Gondwanan glaciation andclimate cooling ~440 million years ago (Sutcliffe et al., 2000;Sheehan, 2001; Finnegan et al., 2011, 2012; Sheets et al.,2016). These phenomena and their consequences associatedwith climate change allow us to explain, at least to a certainextent, the extinction near the Cretaceous-Paleogene boundary(Alvarez et al., 1980, 1981; Schulte et al., 2010; Kaiho et al.,2016), the Triassic-Jurassic extinction event (Marzoli et al.,1999; Whiteside et al., 2010; Blackburn et al., 2013; Percivalet al., 2017), the Late Permian extinction (Wignall et al., 2009),and the extinction near the Ordovician-Silurian boundary(Sutcliffe et al., 2000; Sheehan, 2001; Finnegan et al., 2011,2012; Sheets et al., 2016).

However, it should be noted that the described externalinfluences during these periods are quite diverse and thereis still no single opinion on the causes of known extinctions,especially regarding the Late Devonian extinction ~380 millionyears ago.

Therefore, analysis of another dataset demonstrates thelink between the extinction near the Cretaceous-Paleogeneboundary ~65 million years ago and the sea-level changescaused by movements of the tectonic plates (Peters, 2008) orvolcanic activity (Archibald et al., 2010; Courtillot, Fluteau,2010; Keller et al., 2010; Schoene et al., 2015, 2019).

Some researchers explain the Triassic-Jurassic extinctionevent ~200 million years ago by significant climate warmingas a result of abnormally high concentrations of atmosphericcarbon dioxide of magmatic origin (McElwain et al., 1999;Beerling, 2002; Schaller et al., 2011), which could be accompaniedby storms, lightning strikes and, as a result, fires.The latter could directly cause the global extinction of the terrestrialbiota (Petersen, Lindström, 2012). Some authors denythe link between the global biodiversity loss and changes inatmospheric carbon dioxide concentration during that period(Tanner et al., 2001). Other scientists attribute mass extinctionto the emission of large volumes of volcanic sulphurous gas(Bacon et al., 2013) or to frequent warming and cooling ofthe climate caused by volcanic emissions of large volumes ofsulphurous gas followed by carbon dioxide emission (Guex etal., 2016). Recent studies confirm the great impact of volcanicactivity on the climate change at the end of the Triassic periodand provide evidence that toxic effect of volcanic emissionscan be associated with mercury – the most genotoxic elementon Earth (Percival et al., 2017; Lindström et al., 2019).

Biodiversity loss during the Late Permian ~260 millionyears ago, when more than 90 % of marine invertebrates became extinct, has been explained by various reasons: lowoxygen concentration in the surface layer of the ocean (Knollet al., 1996; Wignall et al., 2009; Shen et al., 2011; Zhang etal., 2018a), including in combination with warm climate whichis harmful to shallow-water organisms (Song et al., 2013);ocean acidification associated with carbon dioxide release intothe atmosphere and the accompanying rapid global warmingand acid rain (Clarkson et al., 2015; Sun et al., 2018); climatecooling, combined with aridity, hypoxia, and acid rain (Zhu etal., 2019). Mathematical modeling of the Late Permian climatesupports the hypothesis that reduced biodiversity during thatperiod could be due to hypoxia and ocean warming (Penn etal., 2018). Recently, additional data in favor of the volcanichypothesis of the biotic crisis in the Late Permian period havebeen obtained (Burgess et al., 2017; Shen et al., 2019).

Biodiversity loss near the Ordovician-Silurian boundary~440 million years ago, when ~85 % of marine organismsbecame extinct, has been traditionally associated with theglobal cooling of the tropical ocean (Sutcliffe et al., 2000;Sheehan, 2001; Finnegan et al., 2011, 2012), which was accompaniedby a drop of the sea level and the loss of shallowhabitats (Finnegan et al., 2012).

According to some researchers, such cooling was triggeredby a significant increase in cosmic dust in the inner space ofthe solar system due to the decay of the L-chondrite parentbody in the asteroid belt ~466 million years ago (Schmitzet al., 2019), while others deny the connection between theasteroid destruction and the level of biodiversity (Lindskoget al., 2017).

Some researcher believe that scenario of the Ordovician-Silurian extinction was more complicated, included three iceages and the cause of the initial extinction was not the seacooling, but the ice melt from glaciers due to the presenceof a large ice cover and a relatively warm ocean during thatperiod causing sea level to rise (Ghienne et al., 2014). Thecause of the second extinction has been considered to be thedecreased oxygen concentration in water that occurred whenthe sea level was high before the glaciation peak in the LateOrdovician period (Bartlett et al., 2018). Nowadays, volcanicactivity is considered to be the cause of the second extinction(Gong et al., 2017; Rasmussen et al., 2019; Smolarek-Lachet al., 2019).

There are many different hypotheses about the cause ofthe Late Devonian extinction ~380 million years ago (Sallan,Coates, 2010), which mainly affected the marine biota, especiallyin shallow water (Ma et al., 2016). Some researchersassociate it with climate cooling (Huang et al., 2018; Wang etal., 2018), which was provoked by the burial of a large amountof organic carbon with a subsequent decrease in atmosphericcarbon dioxide concentration (Huang et al., 2018), and wasaccompanied by the sea-level decrease (Wang et al., 2018).Others attribute the Devonian extinction to global warmingcaused by a massive release of methane gas into the atmosphere,which could be caused by volcanic activity (Gharaieet al., 2004, 2007). And others link it to the frequent climatechange from warming to cooling (Chen et al., 2005), whichwas accompanied by sea level fluctuations (Joachimski, Buggisch,1993) and was provoked by various processes, includingthe burial of a large amount of organic carbon and the dissociation of gas hydrates (Chen et al., 2002). Devonianextinction has also been associated with the spread of fires,the cause of which is considered to be the high concentrationof atmospheric oxygen together with dry climate (Kaiho etal., 2013), trap eruptions (Ricci et al., 2013), asteroid fall(Claeys et al., 1992), etc. It is overall recognized that causesof Devonian extinction are still not clear (Percival et al., 2018).

It is also worth noting the potential uniqueness of bioticcrises during the late Devonian period and near the end of theTriassic period, which were associated not with an increasedextinction rate, but with a decrease in the rate of speciation(Bambach et al., 2004; Lamsdell, Selden, 2017).

As for the remaining documented extinctions: during lateCambrian period ~499 million years ago (Gill et al., 2011),near the end of the Ediacaran period > 540 million years ago(Xiao, Laflamme, 2009; Buatois et al., 2014; Darroch et al.,2015; Zhang et al., 2018b), as well as the loss of biodiversityobserved in the modern period (Barnosky et al., 2011; Ceballoset al., 2015), they have not been associated with globalcatastrophes of an abiotic nature.

Recently, the lack of oxygen in water is more and moreoften considered one of the main causes of global extinctionsof biota, including during the Ediacaran period (Zhang et al.,2018b), during the Late Cambrian period (Gill et al., 2011),near the Ordovician-Silurian boundary (Bartlett et al., 2018),during the late Devonian period (Bond, Wignall, 2008; Liu etal., 2016), at the end of the Permian period (Brennecka et al.,2011; Shen et al., 2011; Lau et al., 2016; Zhang et al., 2018a),and during the early Jurassic period (Them et al., 2018). However,if during the late Permian period the lack of dissolvedoxygen is believed to be a consequence of a global warming(Zhang et al., 2018a), and during the late Ordovician period –a consequence of a climate cooling (Bartlett et al., 2018), whatcould cause it during other periods of mass extinctions is notyet clear. Moreover, there is evidence (Darroch et al., 2015)that contradicts the assertion (Zhang et al., 2018b) of oxygendeficiency in the late Ediacaran ocean.

Periodicity in the history of global extinctions

It is important to note that episodes of mass extinctions onthe Earth are strongly believed to be cyclical, which was firstnoted when creating the first comprehensive database on thefossil record of marine families during the Phanerozoic period(Raup, Sepkoski, 1984, 1986; Sepkoski, 1989). Over a timespan of 250 million years, eight largest extinction-intensitypeaks with a periodic fluctuation in marine biodiversity of~26–27 million years have been detected. Since then, datafrom the Sepkoski’s dataset (Sepkoski, 2002) have beenintensively analyzed using various methods; some authorsreport the presence of a slightly pronounced periodicity ofextinctions of ~27 million years (Lieberman, Melott, 2007),whereas data obtained by other researchers indicate a strictperiodicity of ~62–63 million years (Rohde, Muller, 2005;Lieberman, Melott, 2007), which appeared over an intervalof 500 million years (Rohde, Muller, 2005) (Fig. 1).

Similar studies were conducted using alternative databases:Paleobiology Database (PBDB) of marine invertebrate fossils(Alroy, 2008; Melott, 2008; Lieberman, Melott, 2012; Roberts,Mannion, 2019) and Fossil Record 2 databases for marine and terrestrial fossils (Benton, 1995). Data were obtained both infavor of the presence of periodicity (Melott, 2008; Lieberman,Melott, 2012; Roberts, Mannion, 2019) and against strictcyclicality (Benton, 1995; Alroy, 2008).

In the study (Benton, 1995) seven peaks of mass extinctionsof marine families were identified within the past 250 millionyears with a time interval between them varying from 20 to60 million years. As for the PBDB material, the results of thestudy (Alroy, 2008) did not reveal any evidence in favor ofperiodic extinctions. However, other results confirmed theexistence of a fairly strict periodicity of ~62–63 million yearsin the occurrence of major extinction events in the Phanerozoic(Melott, 2008; Lieberman, Melott, 2012), which was alsoshown in the analysis of the Sepkoski’s dataset (Rohde, Muller,2005; Lieberman, Melott, 2007, 2012). Recent studies of thePaleobiology Database (Roberts, Mannion, 2019) confirm theextinction periodicity of ~27 million years, but limit them tothe last 200 million years. The certainty and significance of thecyclical nature of extinctions with periods of ~27 and ~62 millionyears in the last 465 million years has been demonstratedin other studies (Melott, Bambach, 2014, 2017).

It is necessary to add that one more cycle of marine biodiversitychange with a period of 140 ± 15 million yearswas found in the analyses based on the Sepkoski’s dataset(Rohde, Muller, 2005), but cyclicality of global extinctionsin Phanerozoic with ~62–63 million years period was morestrict.

Hense, based on various databases, researchers have reportedat least three cycles of mass extinctions with periods of26–30, 62–63, and ~140 million years during the Phanerozoiceon (Raup, Sepkoski, 1984, 1986; Sepkoski, 1989; Rohde,Muller, 2005; Lieberman, Melott, 2007, 2012; Melott, 2008;Melott, Bambach, 2014, 2017; Roberts, Mannion, 2019).A cycle with a period of ~27 million years was most clearlymanifested during the last 200 million years (Roberts, Mannion,2019).

In this regard, the question arises – is there a connectionbetween the observed periodicity in the diversity of terrestrial biota and those processes that are considered above to becauses of global extinctions? In other words, is there a periodicabiotic process that could underlie the observed periodicityin the diversity of marine or terrestrial biota or even Earth’sentire biota?

Here it is important to emphasize once again that extinctionsdescribed above are global, that is, they affect almost theentire Earth’s biota, which means that if observed periodicitywas associated with abiotic factors, it could reflect only thoseprocesses that affect the entire planet and are cyclical. Fromthis point of view, two types of processes that have similarcharacteristics can be distinguished. The first are “insideplanetary” processes, that is, they are associated with dynamicprocesses involved in plate tectonic motion that lead tocontinental drift, volcanic activity, changes in sea level, etc.The second are associated with extra-planetary influences andare a reflection of processes associated with the dynamics ofthe planet itself being a space object interacting with otherobjects of the universe.

Let us consider the existing hypotheses on the relationshipbetween the periodicity of global extinctions and global catastrophes,which could be caused by such cyclical processes.

Frequency of extinctionsas a reflection of planetary processesand the evolution of the Sun

Nowadays, there is a number of hypotheses regarding possibleconnection between the periodicity of extinctions onEarth and astronomical processes. For example, a model oflarge-scale fluctuations in the magnetic field of the Sun showsan impressive periodicity of 66 million years (Baker, Flood,2015), which is very close to the periodicity of mass extinctionsof ~62–63 million years identified by analyzing at leasttwo databases of marine invertebrate fossils (Rohde, Muller,2005; Lieberman, Melott, 2007, 2012). Other hypotheseshave been proposed linking frequency of extinctions withfluctuations of extragalactic cosmic-ray intensity as a result ofvertical oscillations of the solar system about the galactic plane (Medvedev, Melott, 2007); with the periodicity of the solarsystem passage through the plane of the Milky Way galaxy(Rampino et al., 1997, 2015; Lieberman, Melott, 2012); andwith the periodicity of the passage of comets near Earth andthe fall of asteroids, which can form different periodicitiesdepending on the size of celestial body (Rampino, Stothers,1984; Rampino et al., 1997).

However, in recent years, new findings indicate that periodicitiesassociated with solar system oscillations about thegalactic plane are statistically unreliable (Erlykin et al., 2017,2018) and could not cause the periodicity of extinctions onEarth. And, although some researchers disagree, it is generallyrecognized that there is no direct evidence of astronomicalreasons for the periodicity of biota extinctions on the planetEarth (Melott, Bambach, 2017).

As for the planetary processes, there is also a wide varietyof opinions. Some researchers explain changes in the fossilizedorganisms by periodic changes in sea level (Peters, 2008;Tennant et al., 2016) or connect them with the dynamics oftectonic movement of continental plates and their fragmentation(Valentine, Moores, 1970; Zaffos et al., 2017). One of theassumptions regarding the fact that tectonic processes on Earthcould cause periodicity of mass extinctions has been basedon the data on the 60-million-year periodicity of seawaterSr87/ Sr86 ratio in marine sediments (Melott et al., 2012).

Other researchers detect a definite correlation between thebiodiversity dynamics and the temperature regime on Earth(Mayhew et al., 2012) and consider periodic global climatechanges to be the cause of extinctions. It can be noted herethat glacial-interglacial cycles on Earth had a periodicity of~135 million years (Veizer et al., 2000), which is statisticallyindistinguishable from the periodicity of 140 ± 15 millionyears, which was revealed based on the Sepkoski’s dataset(Rohde, Muller, 2005).

Of interest is the volcano crater dating over the past 260million years, which demonstrates the cyclicity close to 26–27million years (Rampino, Caldeira, 2015) characteristic of thisparticular period of time (Raup, Sepkoski, 1984, 1986; Sepkoski,1989; Roberts, Mannion, 2019). However, in general,volcanic activity during the last 300 million years is characterizedby weakly manifested cycles with a period of 15, 30,and 60 million years (Prokoph et al., 2004).

As for the rather strict ~62–63 million-years mass-extinctioncycle identified by different researchers using differentdatabases of marine invertebrate fossils (Rohde, Muller,2005; Lieberman, Melott, 2007, 2012; Melott, 2008; Melott,Bambach, 2014, 2017), the existing data on 60-million-yearperiodicity associated with the dynamic processes involved inplate tectonic motion (Melott et al., 2012) and modeling dataon the large-scale fluctuations of the solar magnetic field, bothshow periodicity of 66 million years (Baker, Flood, 2015), butdo not allow strong connection with the periodicity of globalextinctions on Earth.

Several times in the history of biological life on Earth havewe detected serious external influences such as fall of asteroidsand meteorites without subsequent extinction (Archibald etal., 2010), as well as extinctions without abiotic catastrophes,which leads us to an assumption that internal causes of a bioticnature could underlie mass extinctions of biota, which at different periods could coincide with global catastrophes orbe provoked by them. We believe that these internal causesmay be a reflection of a complex dynamic behavior of a livingsystem, such as terrestrial or marine biota, or even the biotaof the entire Earth.

Mass extinctions and their periodicityas a reflection of internal propertiesof a global ecosystem

The idea that fossil biodiversity on Earth is a reflection of theinternal laws of functioning of a global ecosystem, which isthe Earth’s biota, has arisen more than once. Mass extinctions,which have been observed in the Earth’s fossil recordover the past 500 million years and lead to intermittent andirregular evolutionary pace, represent just one aspect of thecomplex dynamic behavior of a global ecosystem. To explainthe phenomenon of punctuated evolution, S.J. Gouldand N. Eldredge have formulated the “theory of punctuatedequilibrium” back in 1972 (Gould, Eldredge, 1977, 1993;Eldredge, Gould, 1997).

This theory is not strict. It is based on “empirical generalizations”of a number of facts that have long been noticed bypaleontologists, which indicate that long periods of evolutionarystability, when species remain almost unchanged,alternate with short intervals of rapid qualitative change,which are characterized by “sudden” extinction of old speciesand subsequently replacement by new types. The authors ofthis theory and other researchers have found quite strikingexamples in the Earth’s fossil record confirming such pattern(Ovcharenko, 1969; Bambach, 1977; Gould, Eldredge, 1977,1993; Williamson, 1981; Sepkoski, 1988; Jackson, Cheetham,1999). Although the interpretation of some studies has beenquestioned (Van Bocxlaer et al., 2008), in general, presence ofsuch pattern in the evolutionary process is not denied (Hunt,2007; Mattila, Bokma, 2008; Rasskin-Gutman, Esteve-Altava,2008).

Previously, the idea of internal biotic causes that determinethe evolutionary dynamics was formulated as “self-organizingcriticality” (Bak, Paczuski, 1995; Sneppen et al., 1995; Solé,Manrubia, 1996), which reflects interactions between differentecosystems and was used to explain mass extinctions and thehypothesis of punctuated evolution. It was assumed that theseinteractions, together with spontaneous mutations and geneticvariations that are always present in populations, could lead tolarge evolutionary rearrangements called the “co-evolutionaryavalanches”. Recently, the concept of “self-organizing criticality”has again attracted the attention of researchers (Nykteret al., 2008; Solé et al., 2010; Hesse, Gross, 2014; Valverde etal., 2015). However, already in the 1990s (Newman, 1997a, b)and later (Alroy, 2008), arguments against this concept havebeen expressed, which were based on the demonstration of thepossibility of mass extinctions using simple models of speciesadaptation to existing conditions and nutrition resourceswithout involvement of co-evolution and critical processes,both with and without influence of the abiotic factors (Roberts,Newman, 1996; Newman, 1997a, b).

There exist other ideas on the internal biotic causes of thebiodiversity on Earth that relate the Phanerozoic biodiversityto the intensity of predation in marine communities (Huntley, Kowalewski, 2007) and suggest a certain role for predators inthe formation of marine biota diversity, although no correlationbetween predators and preys were found in other studies(Madin et al., 2006). Other researchers, seeing a definite relationshipbetween biodiversity and the age of the oceanic crust,connect the history of the seafloor with the biodiversity levelvia the availability of food resources (Cermeño et al., 2017).

In the existing models of the diversity dynamics of thePhanerozoic marine biota that has clear signs of punctuatedevolution in its development, the periodicity of extinctionswas not examined and was introduced into the models as agiven (Markov, 2001a, b; Markov, Korotaev, 2007). However,discussing the modeling results, the authors noted thatthe causes of “staging” should be sought in the structure ofdeveloping communities (Markov, 2001a). A.V. Markov andA.V. Korotaev (2007) paid special attention to those life formsthat have an increased adaptive capacity associated with sexualreproduction. In this regard, we should pay attention to thestudies of A.M. Bush et al. (2016) who believe that diversificationof marine predators starting from the Cretaceous-Cenozoic period (~200 million years ago) can be explainedby the peculiarities of sexual reproduction during the directedtransfer of sperm. However, given that internal fertilization hasprobably developed as early as in the late Neoproterozoic Era(> 500 million years), such delayed diversification requiresan explanation (Novack-Gottshall, 2016).

A number of theoretical studies has connected discontinuityand staging in the Earth’s fossil record with the negative andpositive feedback regulatory loops that a priori exist in nature,and the combination of which leads to system instability(Robertson, 1991; Seaborg, 1999). This property of feedbackregulatory loops has long been noted and was demonstratedin models of biological systems at various levels of their organization(Mackey, Glass, 1977; Decroly, Goldbeter, 1982;Martinez de la Fuente, 1996; Goldbeter et al., 2001; Harish,Hansel, 2015; Likhoshvai et al., 2015, 2016; Kogai et al., 2017;Khlebodarova et al., 2017, 2018). However, it turned out thatthis is not the only mechanism that can cause instability in anonlinear dynamic system.

Periodicity and discontinuityin the history of life viewed throughthe prism of a mathematical model

No one doubts today that models of mathematical physicsare a powerful tool for understanding the deepest laws ofthe Universe. Methods of mathematical modeling do not yetplay such a role in the science of living systems. However,living systems are part of dynamic systems. They are openand non-linear at all levels of their organization, so the methodof mathematical modeling is potentially able to help identifythe laws of their functioning. And, the more global the systemis, the more fundamental and, at the same time, simple in essence,but not in content, should be the laws that determinesystem’s functioning.

To develop the idea of the internal causes of the discontinuityin evolution, we studied the evolution of large ecosystemsusing methods of mathematical modeling. We define largeecosystem as a group of organisms (population) of one species,which we designated as “transit” species. In our models, such population mimics the biota of an ecosystem large enoughto be correlated with terrestrial or marine biota. These aretraditional logistic models of a frame type, in which the efficiencyof reproduction and mortality of organisms dependson population density. According to A.V. Markov, hypothesisthat the dynamics of the Phanerozoic marine biota calculatedby traditional methods(without amendments) adequately reflectsreal changes in biodiversity has not been unproved andremains the most convenient and reliable basis for meaningfulbiological interpretations (Markov, Korotaev, 2007, p. 4).

Evolution is described in models as process of ecosystemself-development (population of a “transit” type), duringwhich there is a local increase in the adaptability of its individualsto the conditions of existence due to mutationalvariability and natural selection.

Analysis of the dynamics of functioning of such modelshave showed that living systems with different reproductionmethods implement different evolutionary laws of selfdevelopment:“asexual” ecosystems showed stasis, whereas“sexual” ecosystems evolved cyclically (Likhoshvai, Khlebodarova,2016; Likhoshvai et al., 2017). That is, it turned outthat if natural selection in a population is directed towardsincreasing the adaptability of its individuals to the conditionsof existence, then, at a certain stage of its evolution (the occurrenceof sexual reproduction), such selection can act asdestabilizing factor.

Moreover, it turned out that these same factors can explainthe peculiarities of punctuated evolution observed in the fossilrecord, such as mass extinctions and phases of rapid diversityincrease, as well as phases of stasis diversity, the causes ofwhich are still not understood (Voje, 2016; Voje et al., 2018).Figure 2 shows evolutionary phases of the density parameterof a “transit” population using one full cycle of the parametervalue fluctuation. In the model, phases of decrease andincrease in the parameter value repeat an unlimited numberof times with approximately the same time interval. The exactduration of each phase cannot be predicted, since the oscillatorydynamics observed in the model is chaotic.

One full evolutionary cycle of a “transit” population iscompleted over time interval t [32,000, 44,000] conv. units,which in the model is ~12,000 conv. units of time (Fig. 2). Theconcept of fractal evolution (Dieckmann, Law, 1996), whichis based on the similarity of laws that regulate the dynamicsof population density, variety of species, genera and higherlevels of organization of living systems at different timescales, allows to transfer these data when changing the timescale according with a level of organization of living systemswith more than a single population. It is easy to verify that ifone conv. unit of time equals 50 years, then duration of oneevolutionary cycle is close to the species lifespan estimate,and if it equals 500 years, we receive an estimate of the genuslifetime, the durations of which are ~0.5 and ~5.9 millionyears, respectively, according to (Gingerich, 1976; Severtsov,1990, 2014). These rough estimates do not prove anything, butsuggest that time scales characteristic of dynamic processesat the level of large ecosystems are one order of magnitudelarger, that is, such time scales range up to tens of millionsof years and cyclic changes in the diversity of Phanerozoicmarine biota with a period of 62–63 million years may represent their reflection (Rohde, Muller, 2005; Lieberman, Melott,2007, 2012; Melott, 2008; Melott, Bambach, 2014, 2017).

Thus, the modeling results have shown that if the efficiencyof reproduction and mortality in a population depends on itsdensity and the most adapted individuals, the genetic diversityof which is a result of genome replication errors duringself-reproduction, are being selected, then these conditionsare sufficient for the formation of cyclical intermittent dynamicsof biodiversity in a living system with sexual type ofreproduction.

The question arises – what is the origin of cyclicality andintermittency observed in the evolution of life on Earth?

Global extinctions in the evolutionary historyof life on Earth as a reflection of the bistabilityphenomenon: the hypothesis of two “trees of life”

The idea that the phenomenon of punctuated evolution canbe based on the bistability in biological systems has beenexpressed by V.A. Likhoshvai long ago in the work dedicatedto the modeling of the evolution of a simple self-developingliving system. It was expressed as an idea of a latent phenotypein a self-developing living system, which represents aninternal resource of its evolutionary development (Likhoshvai,Matushkin, 2000, 2004). Subsequently, when applied to globalecosystems, this idea was transformed into the hypothesis ofthe two “trees of life”.

Here it should be noted that Ch. Darwin defined the diversityof living things on Earth as the “tree of life”. Such comparisonvery accurately reflects the deepest essence of life, whichconstantly gives rise to new thin branches of species duringits continuous evolutionary development that can eventuallyform into new genera, types, classes, etc., but can also dry outand disappear (Darwin, 1991).

The most common characteristics of the “tree of life” arebiota density and species diversity. These characteristics arereflected in our model as the population density of a “transit”species, which at each moment in time depends on the ratiobetween the rates of self-reproduction and mortality of itsindividuals. Analysis of the behaviour of functions that dedescribechanges in these parameters at different time momentsdepending on the density of a “transit” population have shownthat evolving ecosystems with asexual type of reproductionhave only one stable state, while for ecosystems with sexualtype of reproduction the bistability is possible, that is, twostable stationary states, each of which can be interpreted asthe “tree of life”, one of which is being manifested and theother is not. Moreover, if evolution is directed towards improvingthe adaptability of individuals of a “transit” speciesto habitat conditions, which should be accompanied by nicheexpansion and increased utilization of resources, then at somepoint in time the stability of the manifested state becomeslost and the system jumps into a new steady state that existedbefore, but was unmanifested. The result of such transitioncan be interpreted as sudden “disappearance” of old speciesfollowed by explosive appearance of new types, that is, thechange of one “tree of life” to another. From a mathematicalpoint of view, such event is not unusual in dynamic nonlinearsystems. Figure 3 demonstrates the mechanism of local andglobal extinctions depending on the rates of change of functionsdescribing self-reproduction C (red curve) and mortalityD (blue curve) of individuals of a “transit” population atdifferent moments of its evolution.

The intersection of functions C and D corresponds to thestationary states of the system, which can be stable (xmin andxmax) or unstable (xmdl). If current value of density and biodiversityof biota х(t) is located near the stable stationary state,it falls into the region of its attraction and will tend to eitherxmax (see Fig. 3, a, d, e) or xmin (see Fig. 3, c). The fact that atthe same time moment there is one more stable stationary statedoes not affect the state of the system, since x(t) value fallsoutside the region of its attraction and the system cannot getinto it without external influence. Therefore, we can assumethat at the time moment described in Fig. 3, c, stationary statexmin is manifested and stationary state xmax is not. In Fig. 3,a, d, e, on the contrary, stationary state xmax is manifested,whereas stationary state xmin is not.

Since the system evolves over time towards biota sizeand diversity increase, value of the x(t) parameter increases,while the attraction region of the manifested stationary statedecreases and approaches the stationary state xmdl, so that atsome point they merge and disappear. At this time moment weobserve only one stationary state in the system – either xmin(see Fig. 3, b) or xmax (see Fig. 3, f ), which passes from theunmanifested state to the manifested one. Since at this timemoment the x(t) value is significantly different from the valueof the manifested stationary state (see Fig. 3, b, f ), an explosivechange in the x(t) value is observed. We believe that a rapidchange in system parameters during the transition from onestate to another can be a reflection of the uneven evolutionaryrates observed in phylogenetic studies (Nichol et al., 1993;Pagel et al., 2006; Wolf et al., 2006; Palmer et al., 2012).

It also follows from these data that local extinctions (blueoutline) are associated with fluctuations in the current densityand diversity of biota х(t) in the attraction region of the stablestationary state xmax (see Fig. 3, a, d ), while global extinctionsare associated with the loss of stationary state stability and theх(t) transition to the attraction region of the stationary statexmin, which at this time moment becomes single, similar tothat shown in Fig. 3, b. It is this transition that we interpretas the change of one “tree of life” to another.

Thus, we came to the conclusion that adaptation of organismsto the habitat conditions as a result of gradual accumulationof mutations (the evolution) may by itself be one of thecauses of instability in a living system, which manifested itselfas periodically occurring mass extinctions of biota. However,this instability manifested itself only at a certain stage ofthe evolution of living systems and was associated with thedevelopment of sexual dimorphism. This does not contradictwith the fact that during certain periods of life on Earth massextinctions could coincide with planetary environmentaldisasters or be provoked by them.

Conclusion

Analysis of the causes of global extinctions in the Earth’shistory have shown that, although abiogenic factors arerecognized as prevailing and their various combinations canexplain most mass extinctions described in the Earth’s fossilrecord, they do not explain such aspects of the evolutionaryprocess as periodic discontinuity and uneven evolution oflivingorganisms. However, these are evolutionary characteristicsthat are manifested at all known levels of organizationof living systems – from molecular level to biosphere as awhole. It has now been proven that “spasmodicity” of evolutionat the paleontological level is reflected on the molecularlevel (Nichol et al., 1993; Pagel et al., 2006; Wolf et al., 2006;Palmer et al., 2012).

We believe that in addition to external factors, there areother, internal, reasons for the occurrence of global extinctionsof terrestrial biota. According to our hypothesis, theseinternal factors are associated with the phenomenon ofbistability, which occurs only in ecosystems with prevalentsexual reproduction. The fossil record of life on Earth overthe past 500 million years reflects the life history of just suchorganisms. Our hypothesis suggests that even with no globalcatastrophes of an abiotic nature, extinctions in the evolution of living organisms would happen anyway. The possibility ofthis is evidenced by the existence of extinctions that are notyet associated with global catastrophes of an abiotic nature,as well as the evidence of serious external influences thatwere not accompanied by extinctions (Archibald et al., 2010).

We believe that the bistability phenomenon should be manifestedin the evolution of a living system at all levels ofits organization. And at least at the cellular level, we havedemonstrated the contribution of bistability phenomenon tothe evolution of cellular complexity (Likhoshvai, Khlebodarova,2017; Khlebodarova, Likhoshvai, 2018, 2019). Thereis no doubt that at the level of the entire Earth’s biota thebistability phenomenon should interfere with the abiogenicfactors observed in the fossil record of life on Earth. This isevidenced by the extinction cycle with a period of ~140 millionyears, although it was dimly manifested (Rohde, Muller,2005), which can be associated with the frequency of glaciationspreceding extinctions (Veizer et al., 2000); as well asby the extinction cycle with a period close to 26–27 millionyears, which was manifested during the last 250 million years(Raup, Sepkoski, 1984, 1986; Sepkoski, 1989; Roberts, Mannion,2019) and coincided with the dating of volcano craters(Rampino, Caldeira, 2015).

As for the rather strict cyclicity of marine extinctions manifestedover the last 500 million years, the period of which was~63 million years (Rohde, Muller, 2005; Lieberman, Melott,2007, 2012; Melott, 2008; Melott, Bambach, 2014, 2017),both the empirical data on the ~60 million-years periodicity ofthe Sr87/Sr86 ratio change in marine sediments (Melott et al.,2012), which indicates the possibility of cyclicityassociatedwith motion of tectonic plates on Earth, as well as modelingdata on the fluctuations of the Sun’s large-scale magneticfield with the periodicity of 66 million years (Baker, Flood,2015), did not conclusively link them to the periodicity ofglobal extinctions.

At this stage, the modeling results do not explain the existenceof such periodicity of extinctions. For this, the modelis too simple. The dynamics of changes in the biota densityobserved in the model makes it possible to rather roughlyreproduce, with a change in the time scale, the oscillationperiod characteristic of the specific level of organization ofliving systems. However, these estimates suggest that the timescales characteristic of dynamic processes at the level of largeecosystems or even the entire Earth, are tens of millions ofyears. At the moment, this question remains open.

Conflict of interest

The authors declare no conflict of interest.

References

Alroy J. Colloquium paper: dynamics of origination and extinctionin the marine fossil record. Proc. Natl. Acad. Sci. USA. 2008;105(Suppl. 1):11536-11542. DOI 10.1073/pnas.0802597105.

Alvarez L.W., Alvarez W., Asaro F., Michel H.V. Extraterrestrial causefor the Cretaceous-Tertiary extinction. Science. 1980;208(4448):1095-1108.

Alvarez L.W., Alvarez W., Asaro F., Michel H.V. Asteroid extinctionhypothesis. Science. 1981;211(4483):654-656.

Archibald J.D., Clemens W.A., Padian K., Archibald J.D., ClemensW.A., Padian K., Rowe T., Macleod N., Barrett P.M., Gale A.,Holroyd P., Sues H.D., Arens N.C., Horner J.R., Wilson G.P., GoodwinM.B., Brochu C.A., Lofgren D.L., Hurlbert S.H., Hartman J.H.,Eberth D.A., Wignall P.B., Currie P.J., Weil A., Prasad G.V., Dingus L., Courtillot V., Milner A., Milner A., Bajpai S., Ward D.J.,Sahni A. Cretaceous extinctions: multiple causes. Science. 2010;328(5981):973.

Bacon K.L., Belcher C.M., Haworth M., McElwain J.C. Increased atmosphericSO2 detected from changes in leaf physiognomy acrossthe Triassic-Jurassic boundary interval of East Greenland. PLoSOne. 2013;8(4):e60614. DOI 10.1371/journal.pone.0060614.

Bak P., Paczuski M. Complexity, contingency, and criticality. Proc.Natl. Acad. Sci. USA. 1995;92(15):6689-6696.

Baker R.G., Flood P.G. The Sun-Earth connect 3: lessons from theperiodicities of deep time influencing sea-level change and marineextinctions in the geological record. SpringerPlus. 2015;4:285. DOI10.1186/s40064-015-0942-6.

Bambach R.K. Species richness in marine benthic habitats through thePhanerozoic. Paleobiology. 1977;3(2):152-167.

Bambach R.K., Knoll A.J., Wang S.C. Origination, extinction, and massdepletions of marine diversity. Paleobiology. 2004;30:522-542. DOI10.1666/0094-8373(2004)030<0522:OEAMDO>2.0.CO;2.

Barnosky A.D., Matzke N., Tomiya S., Wogan G.O., Swartz B., QuentalT.B., Marshall C., McGuire J.L., Lindsey E.L., Maguire K.C.,Mersey B., Ferrer E.A. Has the Earth’s sixth mass extinction alreadyarrived? Nature. 2011;471(7336):51-57. DOI 10.1038/nature09678.

Bartlett R., Elrick M., Wheeley J.R., Polyak V., Desrochers A., AsmeromY. Abrupt global-ocean anoxia during the Late OrdovicianearlySilurian detected using uranium isotopes of marine carbonates.Proc. Natl. Acad. Sci. USA. 2018;115(23):5896-5901. DOI 10.1073/pnas.1802438115.

Beerling D. CO2 and the end-Triassic mass extinction. Nature. 2002;415(6870):386-387.

Benton M.J. Diversification and extinction in the history of life. Science.1995;268(5207):52-58.

Blackburn T.J., Olsen P.E., Bowring S.A., McLean N.M., Kent D.V.,Puffer J., McHone G., Rasbury E.T., Et-Touhami M. Zircon U-Pbgeochronology links the end-Triassic extinction with the Central AtlanticMagmatic Province. Science. 2013;340(6135):941-945. DOI10.1126/science.1234204.

Bond D.P.G., Wignall P.B. The role of sea-level change and marine anoxiain the Frasnian-Famennian (Late Devonian) mass extinction.Palaeogeogr. Palaeoclimatol. Palaeoecol. 2008;263(3-4):107-118.

Brennecka G.A., Herrmann A.D., Algeo T.J., Anbar A.D. Rapid expansionof oceanic anoxia immediately before the end-Permian massextinction. Proc. Natl. Acad. Sci. USA. 2011;108(43):17631-17634.DOI 10.1073/pnas.1106039108.

Buatois L.A., Narbonne G.M., Mángano M.G., Carmona N.B., MyrowP. Ediacaran matground ecology persisted into the earliest Cambrian.Nat. Commun. 2014;5:3544. DOI 10.1038/ncomms4544.

Burgess S.D., Muirhead J.D., Bowring S.A. Initial pulse of SiberianTraps sills as the trigger of the end-Permian mass extinction. Nat.Commun. 2017;8:164. DOI 10.1038/s41467-017-00083-9.

Bush A.M., Hunt G., Bambach R.K. Sex and the shifting biodiversitydynamics of marine animals in deep time. Proc. Natl. Acad. Sci.USA. 2016;113(49):14073-14078.

Ceballos G., Ehrlich P.R., Barnosky A.D., García A., Pringle R.M.,Palmer T.M. Accelerated modern human-induced species losses:Entering the sixth mass extinction. Sci. Adv. 2015;1(5):e1400253.DOI 10.1126/sciadv.1400253.

Cermeño P., Benton M.J., Paz Ó., Vérard C. Trophic and tectonic limitsto the global increase of marine invertebrate diversity. Sci. Rep.2017;7:15969. DOI 10.1038/s41598-017-16257-w.

Chen D.Z., Qing H.R., Li R.W. The Late Devonian Frasnian-Famennian(F/F) biotic crisis: Insights from delta C-13(carb), delta C-13(org)and Sr-87/Sr-86 isotopic systematics. Earth Planet. Sci. Lett. 2005;235(1-2):151-166.

Chen D.Z., Tucker M.E., Shen Y.N., Yans J., Preat A. Carbon isotopeexcursions and sea-level change: implications for the Frasnian-Famennian biotic crisis. J. Geol. Soc. 2002;59(6):623-626. DOI10.1144/0016-764902-027.

Claeys P., Casier J.G., Margolis S.V. Microtektites and mass extinctions:evidence for a late devonian asteroid impact. Science. 1992;257(5073):1102-1104.

Clarkson M.O., Kasemann S.A., Wood R.A., Lenton T.M., Daines S.J.,Richoz S., Ohnemueller F., Meixner A., Poulton S.W., Tipper E.T.Ocean acidification and the Permo-Triassic mass extinction.Science.2015;348(6231):229-232. DOI 10.1126/science.aaa0193.

Courtillot V., Fluteau F. Cretaceous extinctions: the volcanic hypothesis.Science. 2010;328(5981):973-974.

Darroch S.A., Sperling E.A., Boag T.H., Racicot R.A., Mason S.J.,Morgan A.S., Tweedt S., Myrow P., Johnston D.T., Erwin D.H.,Laflamme M. Biotic replacement and mass extinction of the Ediacarabiota. Proc. Biol. Sci. 2015;282(1814):pii20151003. DOI10.1098/rspb.2015.1003.

Darwin C. The Origin of Species by Means of Natural Selection, or thePreservation of Favoured Races in the Struggle for Life. London,1872. (Russ. ed.: Darvin Ch. Proiskhozhdenie Vidov Putem EstestvennogoOtbora, ili Sokhranenie Blagopriyatnykh Ras v Bor’be zaZhizn’. Saint-Petersburg: Nauka Publ., 1991).

Decroly O., Goldbeter A. Birhythmicity, chaos, and other patterns oftemporal self-organization in a multiply regulated biochemical system.Proc. Natl. Acad. Sci. USA. 1982;79(22):6917-6921.

Dieckmann U., Law R. The dynamical theory of coevolution: a derivationfrom stochastic ecological processes. J. Math. Biol. 1996;34(5-6):579-612.

Eldredge N., Gould S.J. On punctuated equilibria. Science. 1997;276(5311):338-341.

Erlykin A.D., Harper D.A.T., Sloan T., Wolfendale A.W. Mass extinctionsover the last 500 myr: an astronomical cause? Palaeontology.2017;60(2):159-167. DOI 10.1111/pala.12283.

Erlykin A.D., Harper D.A.T., Sloan T., Wolfendale A.W. Periodicityin extinction rates. Palaeontology. 2018;61:149-158. DOI 10.1111/pala.12334.

Finnegan S., Bergmann K., Eiler J.M., Jones D.S., Fike D.A., EisenmanI., Hughes N.C., Tripati A.K., Fischer W.W. The magnitudeand duration of Late Ordovician-Early Silurian glaciation. Science.2011;331(6019):903-906.

Finnegan S., Heim N.A., Peters S.E., Fischer W.W. Climate change andthe selective signature of the Late Ordovician mass extinction. Proc.Natl. Acad. Sci. USA. 2012;109(18):6829-6834.

Gharaie M.H.M., Matsumoto R., Kakuwa Y., Milroy P.G. Late Devonianfacies variety in Iran: volcanism as a possible trigger of theenvironmental perturbation near the Frasnian-Famennian boundary.Geol. Quart. 2004;48(4):323-332.

Gharaie M.H.M., Matsumoto R., Racki G., Kakuwa Y. Chemostratigraphyof Frasnian-Famennian transition: Possibility of methane hydratedissociation leading to mass extinction. Large ecosystem perturbations:causes and consequences. Geological Society of AmericaSpecial Paper. 2007;424:109-125. DOI 10.1130/2007.2424(07).

Ghienne J.F., Desrochers A., Vandenbroucke T.R., Achab A., AsselinE., Dabard M.P., Farley C., Loi A., Paris F., Wickson S., Veizer J.A Cenozoic-style scenario for the end-Ordovician glaciation. Nat.Commun. 2014;5:4485. DOI 10.1038/ncomms5485.

Gill B.C., Lyons T.W., Young S.A., Kump L.R., Knoll A.H., SaltzmanM.R. Geochemical evidence for widespread euxinia in thelater Cambrian ocean. Nature. 2011;469(7328):80-83. DOI 10.1038/nature09700.

Gingerich P.D. Paleontology and phylogeny: patterns of evolution ofthe species level in early tertiary mammals. Am. J. Sci. 1976;276:1-28.Goldbeter A., Gonze D., Houart G., Leloup J.C., Halloy J., Dupont G.From simple to complex oscillatory behavior in metabolic and geneticcontrol networks. Chaos. 2001;11(1):247-260.

Gong Q., Wang X., Zhao L., Grasby S.E., Chen Z.Q., Zhang L., Li Y.,Cao L., Li Z. Mercury spikes suggest volcanic driver of the Ordovician-Silurian mass extinction. Sci. Rep. 2017;13(7(1)):5304. DOI10.1038/s41598-017-05524-5.

Gould S.J., Eldredge N. Punctuated equilibria: the tempo and mode ofevolution reconsidered. Paleobiology. 1977;3:115-151.

Gould S.J., Eldredge N. Punctuated equilibrium comes of age. Nature.1993;366(6452):223-227.

Guex J., Pilet S., Müntener O., Bartolini A., Spangenberg J., Schoene B.,Sell B., Schaltegger U. Thermal erosion of cratonic lithosphere as apotential trigger for mass-extinction. Sci. Rep. 2016;6:23168. DOI10.1038/srep23168.

Harish O., Hansel D. Asynchronous rate chaos in spiking neuronalcircuits. PLoS Comput. Biol. 2015;11(7):e1004266. DOI 10.1371/journal.pcbi.1004266.

Heimdal T.H., Svensen H.H., Ramezani J., Iyer K., Pereira E., RodriguesR., Jones M.T., Callegaro S. Large-scale sill emplacement inBrazil as a trigger for the end-Triassic crisis. Sci. Rep. 2018;8(1):141.DOI 10.1038/s41598-017-18629-8.

Hesse J., Gross T. Self-organized criticality as a fundamental propertyof neural systems. Front. Syst. Neurosci. 2014;8:166. DOI 10.3389/fnsys.2014.00166.

Huang C., Joachimski M.M., Gong Y.M. Did climate changes trigger theLate Devonian Kellwasser Crisis? Evidence from a high-resolutionconodont delta O-18(PO4) record from South China. Earth Planet.Sci. Lett. 2018;495:174-184. DOI 10.1016/j.epsl.2018.05.016.

Huey R.B., Ward P.D. Hypoxia, global warming, and terrestrial latePermian extinctions. Science. 2005;308(5720):398-401.

Hunt G. The relative importance of directional change, random walks,and stasis in the evolution of fossil lineages. Proc. Natl. Acad. Sci.USA. 2007;104(47):18404-18408.

Huntley J.W., Kowalewski M. Strong coupling of predation intensityand diversity in the Phanerozoic fossil record. Proc. Natl. Acad. Sci.USA. 2007;104(38):15006-15010.

Jackson J.B., Cheetham A.H. Tempo and mode of speciation in the sea.Trends Ecol. Evol. 1999;14(2):72-77.

Joachimski M.M., Buggisch W. Anoxic events in the late Frasnian –causes of the Frasnian-Famennian faunal crisis. Geology. 1993;21(8):675-678.

Kaiho K., Oshima N. Site of asteroid impact changed the history oflife on Earth: the low probability of mass extinction. Sci. Rep. 2017;7(1):14855. DOI 10.1038/s41598-017-14199-x.

Kaiho K., Oshima N., Adachi K., Adachi Y., Mizukami T., FujibayashiM., Saito R. Global climate change driven by soot at the K-Pgboundary as the cause of the mass extinction. Sci. Rep. 2016;6:28427. DOI 10.1038/srep28427.

Kaiho K., Yatsu S., Oba M., Gorjan P., Gorjan P., Casier J.G., Ikeda M.A forest fire and soil erosion event during the Late Devonian massextinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2013;392:272-280. DOI 10.1016/j.palaeo.2013.09.008.

Keller G., Adatte T., Pardo A., Bajpai S., Khosla A., Samant B. Cretaceousextinctions: evidence overlooked. Science. 2010;328(5981):974-975. DOI 10.1126/science.328.5981.974-a.

Khlebodarova T.M., Kogai V.V., Fadeev S.I., Likhoshvai V.A. Chaosand hyperchaos in simple gene network with negative feedback andtime delays. J. Bioinform. Comput. Biol. 2017;15(2):1650042. DOI10.1142/S0219720016500426.

Khlebodarova T.M., Kogai V.V., Trifonova E.A., Likhoshvai V.A. Dynamiclandscape of the local translation at activated synapses. Mol.Psychiatry. 2018;23(1):107-114. DOI 10.1038/mp.2017.245.

Khlebodarova T.M., Likhoshvai V.A. Persister cells – a plausible outcomeof neutral coevolutionary drift. Sci. Rep. 2018;8(1):14309.DOI 10.1038/s41598-018-32637-2.

Khlebodarova T.M., Likhoshvai V.A. Molecular mechanisms of noninheritedantibiotic tolerance in bacteria and archaea. Mol. Biol.(Moscow). 2019;53(4):475-483. DOI 10.1134/S0026893319040058.

Knoll A.H., Bambach R.K., Canfield D.E., Grotzinger J.P. ComparativeEarth history and Late Permian mass extinction. Science. 1996;273:452-457.

Kogai V.V., Likhoshvai V.A., Fadeev S.I., Khlebodarova T.M. Multiplescenarios of transition to chaos in the alternative splicingmodel. Int. J. Bifurcat. Chaos. 2017;27(2):1730006. DOI 10.1142/S0218127417300063.

Lamsdell J.C., Selden P.A. From success to persistence: Identifying anevolutionary regime shift in the diverse Paleozoic aquatic arthropodgroup Eurypterida, driven by the Devonian biotic crisis. Evolution.2017;71(1):95-110. DOI 10.1111/evo.13106.

Lau K.V., Maher K., Altiner D., Kelley B.M., Kump L.R., LehrmannD.J., Silva-Tamayo J.C., Weaver K.L., Yu M., Payne J.L. Marineanoxia and delayed Earth system recovery after the end-Permianextinction. Proc. Natl. Acad. Sci. USA. 2016;113(9):2360-2365.DOI 10.1073/pnas.1515080113.

Lieberman B.S., Melott A.L. Considering the case for biodiversity cycles:re-examining the evidence for periodicity in the fossil record.PLoS One. 2007;2(8):e759.

Lieberman B.S., Melott A.L. Whilst this planet has gone cycling on:what role for periodic astronomical phenomena in large-scale patternsin the history of life? In: Talent J.A. (Ed.). Earth and Life, InternationalYear of Planet Earth. Springer Science and Business MediaB.V., 2012;37-50.

Likhoshvai V.A., Fadeev S.I., Khlebodarova T.M. Stasis and periodicityin the evolution of a global ecosystem: the minimum logistic model.Matematicheskaya Biologiya i Bioinformatika = MathematicalBiologyand Bioinformatics. 2017;12(1):120-136. DOI 10.17537/2017.12.120. (in Russian)

Likhoshvai V.A., Khlebodarova T.M. The minimum logistic modelofglobal ecosystem evolution. Proc. of the VI Int. Conf. “MathematicalBiology and Bioinformatics”, Puschino, 16-21 October. 2016;6:116-117. (in Russian)

Likhoshvai V.A., Khlebodarova T.M. Phenotypic variability of bacterialcell cycle: mathematical model. Mathematical Biology and Bioinformatics.2017;12(Suppl.):t23-t44. DOI 10.17537/2017.12.t23.

Likhoshvai V.A., Kogai V.V., Fadeev S.I., Khlebodarova T.M. Alternativesplicing can lead to chaos. J. Bioinform. Comput. Biol. 2015;13(1):1540003. DOI 10.1142/S021972001540003X.

Likhoshvai V.A., Kogai V.V., Fadeev S.I., Khlebodarova T.M. Chaosand hyperchaos in a model of ribosome autocatalytic synthesis. Sci.Rep. 2016;6:38870. DOI 10.1038/srep38870.

Likhoshvai V.A., Matushkin Yu.G. Latent phenotype as adaptation reserve:a simplest model of cell evolution. Proc. of the II Int. Conf.“Bioinformatics of Genome Regulation and Structure”. Novosibirsk.2000;1:195-198.

Likhoshvai V.A., Matushkin Yu.G. Sporadic emergence of latent phenotypeduring evolution. In: Kolchanov N., Hofestaedt R. (Eds.).Bioinformatics of Genome Regulation and Structure. Boston; Dordrecht;London: Kluwer Academic Publishers, 2004;231-243.

Lindskog A., Costa M.M., Rasmussen C.M., Connelly J.N., ErikssonM.E. Refined Ordovician timescale reveals no link between asteroidbreakup and biodiversification. Nat. Commun. 2017;8:14066.DOI 10.1038/ncomms14066.

Lindström S., Sanei H., van de Schootbrugge B., Pedersen G.K., LesherC.E., Tegner C., Heunisch C., Dybkjær K., Outridge P.M. Volcanicmercury and mutagenesis in land plants during the end-Triassicmass extinction. Sci. Adv. 2019;5(10):eaaw4018. DOI 10.1126/sciadv.aaw4018.

Liu J.S., Qie W.K., Algeo T.J., Yao L., Huang J.H., Luo G.M. Changesin marine nitrogen fixation and denitrification rates during the end-Devonian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol.2016;448:195-206. DOI 10.1016/j.palaeo. 2015.10.022.

Ma X.P., Gong Y.M., Chen D.Z., Racki G., Chen X.Q., Liao W.H. The Late Devonian Frasnian-Famennian event in South China – patternsand causes of extinctions, sea level changes, and isotope variations.Palaeogeogr. Palaeoclimatol. Palaeoecol. 2016;448:224-244. DOI10.1016/j.palaeo.2015.10.047.

Mackey M.C., Glass L. Oscillation and chaos in physiological controlsystems. Science. 1977;197:287-289.

Madin J.S., Alroy J., Aberhan M., Fürsich F.T., Kiessling W., KosnikM.A., Wagner P.J. Statistical independence of escalatory ecologicaltrends in Phanerozoic marine invertebrates. Science. 2006;312(5775):897-900.

Markov A.V. A new approach to modeling the diversity dynamics ofPhanerozoic marine biota. Zhurnal Obshchei Biologii = Journal ofGeneral Biology. 2001a;62(6):460-471. (in Russian)

Markov A.V. Dynamics of the marine faunal diversity in the Phanerozoic:a new approach. Paleontol. J. 2001b;35(1):1-9.

Markov A.V., Korotaev A.V. The dynamics of Phanerozoic marine animaldiversity fits the hyperbolic growth model. Zhurnal ObshcheiBiologii = Journal of General Biology. 2007;68(1):3-18. (in Russian)

Martinez de la Fuente I., Martinez L., Veguillas J., Aguirregabiria J.M.Quasiperiodicity route to chaos in a biochemical system. Biophys. J.1996;71(5):2375-2379.

Marzoli A., Renne P.R., Piccirillo E.M., Ernesto M., Bellieni G., DeMin A. Extensive 200-million-year-old continental flood basalts ofthe central atlantic magmatic province. Science. 1999;284(5414):616-618.

T.M., Bokma F. Extant mammal body masses suggest punctuatedequilibrium. Proc. Biol. Sci. 2008;275(1648):2195-2199.DOI 10.1098/rspb.2008.0354.

Mayhew P.J., Bell M.A., Benton T.G., McGowan A.J. Biodiversitytracks temperature over time. Proc. Natl. Acad. Sci. USA. 2012;109(38):15141-15145.

McElwain J.C., Beerling D.J., Woodward F.I. Fossil plants and globalwarming at the Triassic-Jurassic boundary. Science. 1999;285:1386-1390.

Medvedev M.V., Melott A.L. Do extragalactic cosmic rays inducecycles in fossil diversity? Astrophys. J. 2007;664(2):879-889. DOI10.1086/518757.

Melott A.L. Long-term cycles in the history of life: periodic biodiversityin the paleobiology database. PLoS One. 2008;3(12):e4044.DOI 10.1371/journal.pone.0004044.

Melott A.L., Bambach R.K. Analysis of periodicity of extinctionusingthe 2012 geological time scale. Paleobiology. 2014;40:177-196. DOI 10.1666/13047.

Melott A.L., Bambach R.K. Periodicity in the extinction rate and possibleastronomical causes – comment on mass extinctions over thelast 500 myr: an astronomical cause? (Erlykin et al.). Palaeontology.2017;60:911-920. DOI 10.1111/pala.12322.

Melott A.L., Bambach R.K., Petersen K.D., McArthur J.M. An similarto 60-million-year periodicity is common to marine 87Sr/86Sr, fossilbiodiversity, and large-scale sedimentation: what does the periodicityreflect? J. Geol. 2012;120(2):217-226. DOI 10.1086/663877.

Miller C.S., Peterse F., da Silva A.C., Baranyi V., Reichart G.J., KürschnerW.M. Astronomical age constraints and extinction mechanismsof the Late Triassic Carnian crisis. Sci. Rep. 2017;7(1):2557.DOI 10.1038/s41598-017-02817-7.

Newman M.E. A model of mass extinction. J. Theor. Biol. 1997a;189(3):235-252.

Newman M.E. Evidence for self-organized criticality in evolution.Physica D. 1997b;107:293-296.

Nichol S.T., Rowe J.E., Fitch W.M. Punctuated equilibrium and positiveDarwinian evolution in vesicular stomatitis virus. Proc. Natl.Acad. Sci. USA. 1993;90:10424-10428.

Novack-Gottshall P.M. Love, not war, drove the Mesozoic marine revolution.Proc. Natl. Acad. Sci. USA. 2016;113(51):14471-14473. DOI10.1073/pnas.1617404113.

Nykter M., Price N.D., Aldana M., Ramsey S.A., Kauffman S.A.,Hood L.E., Yli-Harja O., Shmulevich I. Gene expression dynamicsin the macrophage exhibit criticality. Proc. Natl. Acad. Sci. USA.2008;105(6):1897-1900. DOI 10.1073/pnas.0711525105.

Ovcharenko V.N. Transitional forms and speciation of brachiopods.Paleontologicheskii Zhurnal = Paleontological Journal. 1969;3:57-63. (in Russian)

Pagel M., Venditti C., Meade A. Large punctuational contribution ofspeciation to evolutionary divergence at the molecular level. Science.2006;314:119-121. DOI 10.1126/science.1129647.

Palmer S.A., Clapham A.J., Rose P., Freitas F.O., Owen B.D., Beresford-Jones D., Moore J.D., Kitchen J.L., Allaby R.G. Archaeogenomicevidence of punctuated genome evolution in Gossypium.Mol. Biol. Evol. 2012;29:2031-2038. DOI 10.1093/molbev/mss070.

Penn J.L., Deutsch C., Payne J.L., Sperling E.A. Temperature-dependenthypoxia explains biogeography and severity of end-Permianmarine mass extinction. Science. 2018;362(6419):eaat1327. DOI10.1126/science.aat1327.

Percival L.M.E., Davies J.H.F.L., Schaltegger U., De Vleeschouwer D.,Da Silva A.C., Föllmi K.B. Precisely dating the Frasnian-Famennianboundary: implications for the cause of the Late Devonian massextinction.Sci. Rep. 2018;8(1):9578. DOI 10.1038/s41598-018-27847-7.

Percival L.M.E., Ruhl M., Hesselbo S.P., Jenkyns H.C., Mather T.A.,Whiteside J.H. Mercury evidence for pulsed volcanism during theend-Triassic mass extinction. Proc. Natl. Acad. Sci. USA. 2017;114(30):7929-7934. DOI 10.1073/pnas.1705378114.

Peters S.E. Environmental determinants of extinction selectivity inthe fossil record. Nature. 2008;454(7204):626-629. DOI 10.1038/nature07032.

Petersen H.I., Lindström S. Synchronous wildfire activity rise and miredeforestation at the Triassic-Jurassic boundary. PLoS One. 2012;7(10):e47236. DOI 10.1371/journal.pone.0047236.

Prokoph A., Ernst R.E., Buchan K.L. Time-series analysis of large igneousprovinces: 3500 Ma to present. J. Geol. 2004;112(1):1-22.DOI 10.1086/379689.

Rampino M.R. Disc dark matter in the Galaxy and potential cyclesof extraterrestrial impacts, mass extinctions and geological events.MNRAS. 2015;448(2):1816-1820. DOI 10.1093/mnras/stu2708.

Rampino M.R., Caldeira K. Periodic impact cratering and extinctionevents over the last 260 million years. MNRAS. 2015;454(4):3480-3484. DOI 10.1093/mnras/stv2088.

Rampino M.R., Haggerty B.M., Pagano T.C. A unified theory of impactcrises and mass extinctions: quantitative tests. Ann. N.Y. Acad. Sci.1997;822:403-431.

Rampino M.R., Rodriguez S., Baransky E., Cai Y. Global nickelanomaly links Siberian Traps eruptions and the latest Permian massextinction. Sci. Rep. 2017;7(1):12416. DOI 10.1038/s41598-017-12759-9.

Rampino M.R., Stothers R.B. Geological rhythms and cometary impacts.Science. 1984;226:1427-1431.

Rasmussen C.M.Ø., Kröger B., Nielsen M.L., Colmenar J. Cascadingtrend of Early Paleozoic marine radiations paused by Late Ordovicianextinctions. Proc. Natl. Acad. Sci. USA. 2019;116(15):7207-7213. DOI 10.1073/pnas.1821123116.

Rasskin-Gutman D., Esteve-Altava B. The multiple directions of evolutionarychange. Bioessays. 2008;30(6):521-525. DOI 10.1002/bies.20766.

Raup D.M., Sepkoski J.J. Jr. Mass extinctions in the marine fossil record.Science. 1982;215(4539):1501-1503.

Raup D.M., Sepkoski J.J. Periodicity of extinctions in the geologic past.Proc. Natl. Acad. Sci. USA. 1984;81(3):801-805.

Raup D.M., Sepkoski J.J. Jr. Periodic extinction of families and genera.Science. 1986;231:833-836.

Ricci J., Quidelleur X., Pavlov V., Orlov S., Shatsillo A., Courtillot V.New 40Ar/39Ar and K-Ar ages of the Viluy traps (Eastern Siberia):Further evidence for a relationship with the Frasnian-Famennianmass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 2013;386:531-540. DOI 10.1016/j.palaeo.2013.06.020.

Roberts B.W., Newman M.E. A model for evolution and extinction.J. Theor. Biol. 1996;180(1):39-54.

Roberts G.G., Mannion P.D. Timing and periodicity of Phanerozoicmarine biodiversity and environmental change. Sci. Rep. 2019;9(1):6116. DOI 10.1038/s41598-019-42538-7.

Robertson D.S. Feedback theory and Darwinian evolution. J. Theor.Biol. 1991;152(4):469-484.

Rohde R.A., Muller R.A. Cycles in fossil diversity. Nature. 2005;434(7030):208-210.

Sallan L.C., Coates M.I. End-Devonian extinction and a bottleneckin the early evolution of modern jawed vertebrates. Proc. Natl.Acad. Sci. USA. 2010;107(22):10131-10135. DOI 10.1073/pnas.0914000107.

Schaller M.F., Wright J.D., Kent D.V. Atmospheric PCO2 perturbationsassociated with the Central Atlantic Magmatic Province. Science.2011;331(6023):1404-1409. DOI 10.1126/science.1199011.

Schmitz B., Farley K.A., Goderis S., Heck P.R., Bergström S.M., BoschiS., Claeys P., Debaille V., Dronov A., van Ginneken M., HarperD.A.T., Iqbal F., Friberg J., Liao S., Martin E., Meier M.M.M.,Peucker-Ehrenbrink B., Soens B., Wieler R., Terfelt F. An extraterrestrialtrigger for the mid-Ordovician ice age: Dust from the breakupof the L-chondrite parent body. Sci. Adv. 2019;5(9):eaax4184.DOI 10.1126/sciadv.aax4184.

Schoene B., Eddy M.P., Samperton K.M., Keller C.B., Keller G.,Adatte T., Khadri S.F.R. U-Pb constraints on pulsed eruption of theDeccan Traps across the end-Cretaceous mass extinction. Science.2019;363(6429):862-866. DOI 10.1126/science.aau2422.

Schoene B., Samperton K.M., Eddy M.P., Keller G., Adatte T., BowringS.A., Khadri S.F., Gertsch B. U-Pb geochronology of theDeccan Traps and relation to the end-Cretaceous mass extinction.Science. 2015;347(6218):182-184. DOI 10.1126/science.aaa0118.

Schulte P., Alegret L., Arenillas I., Arz J.A., Barton P.J., Bown P.R.,Bralower T.J., Christeson G.L., Claeys P., co*ckell C.S., CollinsG.S., Deutsch A., Goldin T.J., Goto K., Grajales-Nishimura J.M.,Grieve R.A., Gulick S.P., Johnson K.R., Kiessling W., Koeberl C.,Kring D.A., MacLeod K.G., Matsui T., Melosh J., Montanari A.,Morgan J.V., Neal C.R., Nichols D.J., Norris R.D., PierazzoE.,Ravizza G., Rebolledo-Vieyra M., Reimold W.U., RobinE., SalgeT., Speijer R.P., Sweet A.R., Urrutia-Fucugauchi J., VajdaV.,Whalen M.T., Willumsen P.S. The Chicxulub asteroid impact andmass extinction at the Cretaceous-Paleogene boundary. Science.2010;327(5970):1214-1218. DOI 10.1126/science.1177265.

Seaborg D.M. Evolutionary feedback: a new mechanism for stasis andpunctuated evolutionary change based on integration of the organism.J. Theor. Biol. 1999;198(1):1-26.

Sepkoski J.J. Jr. Extinctions of life. Los Alamos Sci. 1988;16:36-49.Sepkoski J.J. Jr. Periodicity in extinction and the problem of catastrophismin the history of life. J. Geol. Soc. London. 1989;146:7-19.

Sepkoski J.J. Jr. A compendium of fossil marine animal genera. Bull.Am. Paleontol. 2002;363:1-560.

Severtsov A.S. Interspecific variety as a cause of evolutionary stability.Zhurnal Obshchei Biologii = Journal of General Biology. 1990;51(5):579-589. (in Russian)

Sheehan P.M. The Late Ordovician mass extinction. Annu. Rev. EarthPlanet. Sci. 2001;29:331-364.

Sheets H.D., Mitchell C.E., Melchin M.J., Loxton J., Štorch P., CarlucciK.L., Hawkins A.D. Graptolite community responses to globalclimate change and the Late Ordovician mass extinction. Proc.Natl. Acad. Sci. USA. 2016;113(30):8380-8385. DOI 10.1073/pnas.1602102113.

Shen J., Chen J., Algeo T.J., Yuan S., Feng Q., Yu J., Zhou L.,O’Connell B., Planavsky N.J. Evidence for a prolonged Permian-Triassic extinction interval from global marine mercury records.Nat. Commun. 2019;10(1):1563. DOI 10.1038/s41467-019-09620-0.

Shen Y., Farquhar J., Zhang H., Masterson A., Zhang T., Wing B.A.Multiple S-isotopic evidence for episodic shoaling of anoxic waterduring Late Permian mass extinction. Nat. Commun. 2011;2:210.DOI 10.1038/ncomms1217

Smolarek-Lach J., Marynowski L., Trela W., Wignall P.B. Mercuryspikes indicate a volcanic trigger for the Late Ordovician mass extinctionevent: an example from a deep shelf of the Peri-Baltic region.Sci. Rep. 2019;9(1):3139. DOI 10.1038/s41598-019-39333-9.

Sneppen K., Bak P., Flyvbjerg H., Jensen M.H. Evolution as a selforganizedcritical phenomenon. Proc. Natl. Acad. Sci. USA. 1995;92:5209-5213.

Solé R.V., Manrubia S.C. Extinction and self-organized criticality in amodel of large-scale evolution. Phys. Rev. E. 1996;54(1):R42-R45.

Solé R.V., Saldaña J., Montoya J.M., Erwin D.H. Simple model of recoverydynamics after mass extinction. J. Theor. Biol. 2010;267(2):193-200. DOI 10.1016/j.jtbi.2010.08.015.

Song H., Wignall P.B., Chu D., Tong J., Sun Y., Song H., He W., Tian L.Anoxia/high temperature double whammy during the Permian-Triassicmarine crisis and its aftermath. Sci. Rep. 2014;4:4132. DOI10.1038/srep04132.

Sun H., Xiao Y., Gao Y., Zhang G., Casey J.F., Shen Y. Rapid enhancementof chemical weathering recorded by extremely light seawaterlithium isotopes at the Permian-Triassic boundary. Proc. Natl. Acad.Sci. USA. 2018;115(15):3782-3787. DOI 10.1073/pnas.1711862115.

Sutcliffe O.E., Dowdeswell J.A., Whittington R.J., Theron J.N., Craig J.Calibrating the Late Ordovician glaciation and mass extinctionby the eccentricity cycles of Earth’s orbit. Geology. 2000;28(11):967-970. DOI 10.1130/0091-7613(2000)028<0967:CTLOGA>2.3.CO;2.

Tanner L.H., Hubert J.F., Coffey B.P., McInerney D.P. Stability of atmosphericCO2 levels across the Triassic/Jurassic boundary. Nature.2001;411(6838):675-677.

Tennant J.P., Mannion P.D., Upchurch P. Sea level regulated tetrapoddiversity dynamics through the Jurassic/Cretaceous interval. Nat.Commun. 2016;7:12737. DOI 10.1038/ncomms12737.

Them T.R. 2nd, Gill B.C., Caruthers A.H., Gerhardt A.M., Gröcke D.R.,Lyons T.W., Marroquín S.M., Nielsen S.G., Trabucho Alexandre J.P.,Owens J.D. Thallium isotopes reveal protracted anoxia during theToarcian (Early Jurassic) associated with volcanism, carbon burial,and mass extinction. Proc. Natl. Acad. Sci. USA. 2018;115(26):6596-6601. DOI 10.1073/pnas.1803478115.

Thibodeau A.M., Ritterbush K., Yager J.A., West A.J., Ibarra Y., BottjerD.J., Berelson W.M., Bergquist B.A., Corsetti F.A. Mercuryanomalies and the timing of biotic recovery following the end-Triassicmass extinction. Nat. Commun. 2016;7:11147. DOI 10.1038/ncomms11147.

Valentine J.W., Moores E.M. Plate-tectonic regulation of faunal diversityand sea level: a model. Nature. 1970;228:657-659.

Valverde S., Ohse S., Turalska M., West B.J., Garcia-Ojalvo J. Structuraldeterminants of criticality in biological networks. Front. Physiol.2015;6:127. DOI 10.3389/fphys.2015.00127.

Van Bocxlaer B., Damme D.V., Feibel C.S. Gradual versus punctuatedequilibrium evolution in the Turkana Basin molluscs: evolutionaryevents or biological invasions? Evolution. 2008;62(3):511-520. DOI10.1111/j.1558-5646.2007.00296.x.

Veizer J., Godderis Y., Francois L. Evidence for decoupling of atmosphericCO2 and global climate during the Phanerozoic eon. Nature.2000;408:698-701. DOI 10.1038/35047044.

Voje K.L. Tempo does not correlate with mode in the fossil record. Evolution.2016;70(12):2678-2689. DOI 10.1111/evo.13090.

Voje K.L., Starrfelt J., Liow L.H. Model adequacy and microevolutionaryexplanations for stasis in the fossil record. Am. Nat. 2018;191(4):509-523. DOI 10.1086/696265.

Wang X., Liu S.A., Wang Z.R., Chen D.Z., Zhang L.Y. Zinc and strontiumisotope evidence for climate cooling and constraints on theFrasnian-Famennian (similar to 372 Ma) mass extinction. Palaeogeogr.Palaeoclimatol. Palaeoecol. 2018;498:68-82. DOI 10.1016/j.palaeo.2018.03.002.

Whiteside J.H., Olsen P.E., Eglinton T., Brookfield M.E., SambrottoR.N. Compound-specific carbon isotopes from Earth’s largestflood basalt eruptions directly linked to the end-Triassic mass extinction.Proc. Natl. Acad. Sci. USA. 2010;107(15):6721-6725. DOI10.1073/pnas.1001706107.

Wignall P.B., Sun Y., Bond D.P., Izon G., Newton R.J., Védrine S.,Widdowson M., Ali J.R., Lai X., Jiang H., Cope H., Bottrell S.H. Volcanism, mass extinction, and carbon isotope fluctuations in theMiddle Permian of China. Science. 2009;324(5931):1179-1182.DOI 10.1126/science.1171956.

Williamson P.O. Palaeontological documentation of speciation in Cenozoicmolluscs from Turkana basin. Nature. 1981;293:437-443.

Wolf Y.I., Viboud C., Holme E.C., Koonin E.V., Lipman D.J. Longintervals of stasis punctuated by bursts of positive selection in theseasonal evolution of influenza A virus. Biol. Direct. 2006;1:34. DOI10.1186/1745-6150-1-34.

Xiao S., Laflamme M. On the eve of animal radiation: phylogeny, ecologyand evolution of the Ediacara biota. Trends Ecol. Evol. 2009;24(1):31-40.

Zaffos A., Finnegan S., Peters S.E. Plate tectonic regulation of globalmarine animal diversity. Proc. Natl. Acad. Sci. USA. 2017;114(22):5653-5658. DOI 10.1073/pnas.1702297114.

Zhang F., Romaniello S.J., Algeo T.J., Lau K.V., Clapham M.E.,Richoz S., Herrmann A.D., Smith H., Horacek M., Anbar A.D. Multipleepisodes of extensive marine anoxia linked to global warmingand continental weathering following the latest Permian massextinction. Sci. Adv. 2018a;4(4):e1602921. DOI 10.1126/sciadv.1602921.

Zhang F., Xiao S., Kendall B., Romaniello S.J., Cui H., Meyer M., GilleaudeauG.J., Kaufman A.J., Anbar A.D. Extensive marine anoxiaduring the terminal Ediacaran Period. Sci. Adv. 2018b;4(6):eaan8983.DOI 10.1126/sciadv.aan8983.

Zhu Z., Liu Y., Kuang H., Benton M.J., Newell A.J., Xu H., An W.,Ji S., Xu S., Peng N., Zhai Q. Altered fluvial patterns in North Chinaindicate rapid climate change linked to the Permian-Triassic massextinction. Sci. Rep. 2019;9(1):16818. DOI 10.1038/s41598-019-53321-z.

Acknowledgments

The study was carried out with the financial support of the Russian Foundation for Basic Research in the framework of the scientificproject 19-14-50159. The authors are grateful to V.V. Suslov for critical comments and useful discussions during manuscript preparation and T. Kalymbetovafor the translation of the article from Russian into English.

Contributor Information

T.M. Khlebodarova, Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia.

V.A. Likhoshvai, Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia.