Confirmation of Romer's Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization

Abstract

The first terrestrialization of species that evolved from previously aquatic taxa was a seminal event in evolutionary history. For vertebrates, one of the most important terrestrialized groups, this event was interrupted by a time interval known as Romer's Gap, for which, until recently, few fossils were known. Here, we argue that geochronologic range data of terrestrial arthropods show a pattern similar to that of vertebrates. Thus, Romer's Gap is real, occupied an interval from 360 million years before present (MYBP) to 345 MYBP, and occurred when environmental conditions were unfavorable for air-breathing, terrestrial animals. These model results suggest that atmospheric oxygen levels were the major driver of successful terrestrialization, and a low-oxygen interval accounts for Romer's Gap. Results also show that terrestrialization among members of arthropod and vertebrate clades occurred in two distinct phases. The first phase was a 65-million-year ( (1) indicates that arthropods, with species interpreted as fully land-based before 400 million years before present (MYBP) (2), preceded vertebrates onto land by tens of millions of years. The first body fossils identified as stegocephalians (limbed vertebrates) are known from strata Ϸ370 MYBP, such that the appearance of the limb with digits, the loss of the opercular apparatus, and the development of other characters that subsequently allowed a terrestrial lifestyle, presumably occurred during the 25-My interval between 385 and 360 MYBP (3, 4). Most of our understanding about these crucial vertebrate events comes from only a few freshwater deposits from Euramerican localities, with outcrops in Greenland producing the most prolific stegocephalian remains. Elginerpeton and Obruchevichthys were first, between 385 and 375 MYBP, followed several million years later by a modest radiation that included Ventastega, Ichythostega, Acanthostega, Tulerpeton, Metaxygnathus, and Hynerpeton. Although most of these taxa possessed limbs (although this is not certain for Elginerpeton and Obruchevichthys), all of these taxa have been interpreted as fully aquatic, rather than terrestrial (5-7). Their respiratory systems are poorly known, but osteology suggests that they were able to derive some amount of O 2 from water instead of being entirely air breathing (8). These stegocephalians disappeared soon thereafter, followed rapidly by rare appearances of limbed vertebrates. This temporal gap has long been called Romer's Gap, and until recently it was unknown whether this hiatus was due to a combination of unfavorable taphonomic conditions and collection failure or whether it represented an interval of intrinsically low diversity and an abundance of limbed vertebrates. Romer's Gap separates occurrences of the earliest (Late Devonian) aquatic stegocephalians from a much larger adaptive radiation that included the first terrestrial vertebrates that commenced during the Visean stage of the Early Carboniferous. Although new collections have partly filled Romer's Gap (9), including the d...

Arthropod cuticles from the upper Viséan (Mississippian) of eastern Germany

“…This period is generally known as Romer's Gap. It has been hypothesized that the absence of terrestrial arthropods and tetrapods is related to low oxygen levels, which inhibited these animals with poorly developed respiratory structures from leaving the water (Ward et al 2006). Whether this hypothesis can be maintained or whether the absence of terrestrial fauna is …”

“…The Brigantian (late Viséan) marks the start of an increased radiation of terrestrial arthropods (Ward et al 2006) and tetrapods (Smithson et al 2012) after a time interval reaching from the latest Devonian to the Holkerian (~middle Viséan) that is characterized by a general absence of terrestrial arthropods and tetrapods. This period is generally known as Romer's Gap.…”

Alterações Climáticas, Perceções e Racionalidades

“…A construção progressiva desta camada protetora de ozono, a partir de há uns 2 mil Ma (e.g., Glikson, 2014;Maruyamab et al, 2014) ou mesmo antes, talvez há cerca de 2,6 Ma (Watanabe et al, 2000;Cockell & Raven, 2007), juntamente com o enriquecimento da atmosfera em oxigénio, permitiu que as formas de vida migrassem até às camadas superficiais do oceano, viabilizando a proliferação do fitoplâncton, sendo mesmo possível que, nessa altura, tivessem ocorrido as primeiras tentativas de colonização de áreas emersas (Cockell & Raven, 2007). Há cerca de mil Ma ocorreu outro GOE, normalmente conhecido por Evento Neoproterozoico de Oxigenação (e.g., Ward et al, 2006;Shields-Zhou & Och, 2010), que, progressivamente, criou condições para que, mais tarde, com início há cerca de 600 Ma, se verificasse o aparecimento de forma complexas de vida, cuja "explosão" se verificou no Câmbrico, há cerca de 541 (e.g., Marshall, 2006;Butterfield, 2007;BaudouinCornu & Thomas, 2007). Depois dessa altura, o oxigénio atmosférico continuou a ser um fator determinante na progressiva adaptação da vida, nomeadamente dos artrópodes e vertebrados, aos ambientes terrestres (e.g., Ward et al, 2006;Baudouin-Cornu & Thomas, 2007).…”

“…Há cerca de mil Ma ocorreu outro GOE, normalmente conhecido por Evento Neoproterozoico de Oxigenação (e.g., Ward et al, 2006;Shields-Zhou & Och, 2010), que, progressivamente, criou condições para que, mais tarde, com início há cerca de 600 Ma, se verificasse o aparecimento de forma complexas de vida, cuja "explosão" se verificou no Câmbrico, há cerca de 541 (e.g., Marshall, 2006;Butterfield, 2007;BaudouinCornu & Thomas, 2007). Depois dessa altura, o oxigénio atmosférico continuou a ser um fator determinante na progressiva adaptação da vida, nomeadamente dos artrópodes e vertebrados, aos ambientes terrestres (e.g., Ward et al, 2006;Baudouin-Cornu & Thomas, 2007). Após o Câmbrico, a composição da atmosfera nunca mais sofreu variações extremas, embora as quantidades relativas dos seus componentes tenham conhecido variações notáveis em função de um conjunto complexo de fatores, entre os quais, as glaciações, a geometria dos continentes, as erupções vulcânicas, as áreas cobertas por vegetação e os impactos meteoríticos.…”

Delayed fungal evolution did not cause the Paleozoic peak in coal production

“…More recently, the evolution of lignin degradation in basidiomycete fungi was traced via phylogenomic methods and relaxed molecular clock estimates to the Permian (13,14), offering support for a fungi-mediated decrease in coal formation following the Carboniferous (13). The wholesale or partial attribution of the Carboniferous−Permian peak in coal production to this evolutionary lag between lignin synthesis and fungal degradation of lignin has been widely promulgated (8,(15)(16)(17)(18)(19)(20)(21)(22), reflecting the growing interest in life−Earth feedbacks over geological timescales (23)(24)(25)(26)(27)(28). Such geobiological hypotheses sometimes persist based largely on the strength of their novelty, without sufficient predictive testing.…”