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DIVERSITY CHANGE...

Diversity change during the rise of tetrapods and the impact of the 'Carboniferous rainforest collapse'Abstract

The 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. Introduction

Tetrapods (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 Methods

Newly 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.