Diversity change during the rise of tetrapods and the impact of the 'Carboniferous rainforest collapse'AbstractThe Carboniferous and early Permian were critical intervals in the diversification of early four-limbed vertebrates (tetrapods), yet the major patterns of diversity and biogeography during this time remain unresolved. Previous estimates suggest that global tetrapod diversity rose continuously across this interval and that habitat fragmentation following the 'Carboniferous rainforest collapse' (CRC) drove increased endemism among communities. However, previous work failed to adequately account for spatial and temporal biases in sampling. Here, we reassess early tetrapod diversity and biogeography with a new global species-level dataset using sampling standardization and network biogeography methods. Our results support a tight relationship between observed richness and sampling, particularly during the Carboniferous. We found that subsampled species richness initially increased into the late Carboniferous, then decreased substantially across the Carboniferous/Permian boundary before slowly recovering in the early Permian. Our analysis of biogeography does not support the hypothesis that the CRC drove endemism; instead, we found evidence for increased cosmopolitanism in the early Permian. While a changing environment may have played a role in reducing diversity in the earliest Permian, our results suggest that the CRC was followed by increased global connectivity between communities, possibly reflecting both reduced barriers to dispersal and the diversification of amniotes.1. IntroductionTetrapods (four-limbed vertebrates) first appeared on land in the late Devonian and during the Carboniferous and early Permian established the first terrestrial vertebrate communities. In the early Carboniferous, these amphibian-like early tetrapods radiated rapidly and diversified into a wide variety of morphologies and sizes. Later in the Carboniferous, crown amniotes appeared, and by the early Permian, the terrestrial vertebrate fauna was dominated by synapsids (the mammalian stem-group), such as edaphosaurids and sphenacodontids, alongside a diverse array of basal reptiles (e.g. captorhinids) and amphibians.This diversification occurred as the surrounding environment was transitioning from wetlands in the Carboniferous to more arid conditions in the Permian. During the late Carboniferous, Euramerica (Europe and North America) lay at the equator and was predominantly covered by tropical rainforests, commonly referred to as the 'Coal Forests'. During the Kasimovian (approx. 303-307 Ma), these rainforests began to disappear from large parts of the globe, and by the early Permian had been replaced in many regions by dryland vegetation as a more arid climate developed. This 'rainforest collapse' culminated in what is considered one of two mass extinction events evident in the plant fossil record.Despite this interval being a crucial time for tetrapod evolution and the establishment of terrestrial ecosystems, few studies have focused on Carboniferous-early Permian tetrapod diversity patterns or have attempted to quantify the impact of the 'Carboniferous rainforest collapse' (CRC) on the terrestrial vertebrate fauna. Instead, most work has been focused on the later end-Permian mass extinction and more recently on the early and mid-Permian extinction events. A previous study that attempted to assess the impact of the CRC suggested that the newly fragmented habitats following the collapse drove the development of endemism among tetrapod communities. This is proposed to have led to reduced local richness (alpha diversity) but higher global diversity (gamma diversity) following the CRC. However, this study failed to adequately account for how sampling of the fossil record varies in both time and space, largely accepting raw diversity patterns at face value. Moreover, the analysis was conducted using a family-level dataset, rather than one at species level, and some of the data used in this study are no longer accessible.The impact of uneven sampling on estimates of diversity has been appreciated for almost half a century, and in recent years there have been an increasing number of studies investigating the influences of sampling biases on palaeodiversity. The correlation between palaeodiversity and sampling has been repeatedly demonstrated in many fossil groups, including terrestrial vertebrates, marine vertebrates, insects, marine invertebrates and plants. Sampling intensity is influenced by several factors including geographical location, volume and variety of preserved sedimentary environments, collection methods and academic interest. Substantial efforts have been made recently to develop statistical methods which can mitigate these biases allowing diversity to be estimated from an incomplete fossil record.Here, using a newly compiled global species-level dataset alongside sampling standardization and network biogeography methods, we investigate patterns of early tetrapod diversity and biogeography from the Carboniferous to early Permian to answer the following questions. (i) What are the major patterns of tetrapod diversity during this interval? (ii) How do sampling biases impact estimates of diversity, and how can we best account for them? (iii) Did the 'CRC' drive the development of endemism among tetrapod communities?2. Material and MethodsNewly compiled data detailing the global occurrences of early tetrapod species from the beginning of the Carboniferous (Tournaisian) to the end of the Cisuralian epoch (Kungurian), informally referred to as the 'early Permian', were downloaded from the Paleobiology Database (paleobiodb.org, accessed 19 September 2017). These data result from a concerted effort to document the Palaeozoic terrestrial tetrapod fossil record, led by the lead author of this study. The data represent the current published knowledge on the global occurrences and taxonomic opinions of early tetrapods. Data preparation and analyses were conducted within R v. 3.4.5. All marine taxa and ichnotaxa were discarded from the dataset, and the final cleaned dataset comprises 476 tetrapod species from 385 collections (= fossil localities), totalling 1047 unique global occurrences.