The evolution of mesic biomes: insights from an ancient lineage of arachnids

382 Pages·2016·11.72 MB·English

by  Danilo Harms

The evolution of mesic biomes: insights from
an ancient lineage of arachnids

Danilo Harms
BSc Biology; MSc Zoology

School of Animal Biology
The University of Western Australia

This thesis is presented for the degree of Doctor of Philosophy of
The University of Western Australia

December 2014
Cover Page.
A selection of Pseudotyrannochthoniidae habitats across the world: mesophytic forest at the
Fuwa-no-Taki Waterfall (Japan, left), a streambed in the Mostyn Hardy Cave (Tasmania,
middle), and wet sclerophyllous forest in the Dandenong Ranges (mainland Australia, right).
Pseudotyrannochthonius sp. ‘TAS-9’ is a currently undescribed species and endemic to Mostyn
Hardy Cave. It is one of more than 200 putative species proposed in this thesis that have yet to
be named.
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NIHIL IN TERRA SINE CAUSA FIT.

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Dedication

This thesis is dedicated to my granddads, Wolfgang and Hermann, for
sparking my keen interest in all things living, and for letting me play in
the cornfields and forests when I was a boy.

This thesis would not exist without your encouragement back then!

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Summary

I investigated the evolutionary history of pseudoscorpions in the family
Pseudotyrannochthoniidae from global to local scales, using molecular sequence data
from samples spanning the full spectrum of morphological diversity and geographic
distributions. I combined phylogenetic reconstruction, molecular dating, distribution-
and environmental niche modelling with population genetics and taxonomy to unravel
the evolutionary history of this fauna.

This is an ancient lineage with origins in the Triassic-Jurassic on the supercontinent
Pangaea. Although the phylogeny reflects the split of this gigantic landmass into
Laurasia (Northern) and Gondwana (Southern), cladogeneses within continents are
often older than tectonic separation, indicating that diversification has been caused by
factors other than tectonic rifting.

The Australian fauna is polyphyletic and falls into five distinct genetic lineages: a) two
monotypic lineages from caves in Tasmania, b) an ’eastern’ lineage widespread in
mesic habitats along the east coast and in southeastern Australia, c) a ‘southeastern’
lineage from alpine habitats and caves, and d) a ‘southwestern’ lineage. There are
ancient links: two groups from caves in Tasmania nest with forms from South America,
consistent with long-term persistence of Gondwanan lineages in buffered habitats.
Primary diversification of the remaining lineages coincides with periods of drastic
climate change during the Mio-Pliocene in Australia that lead to widespread
contraction and fragmentation of mesic habits.

The ‘eastern’ lineage within the Australian fauna, comprised of more than 70 species, is
widespread in all mesic climate and vegetation zones. This fauna is divided along
climatic and latitudinal gradients: two sympatric lineages in the cool temperate
southeast – one ranging north from Tasmania to the Australian Alps, two lineages in
southern and northern warm temperate New South Wales, and two lineages in
subtropical and tropical Queensland. These divisions generally correspond with major
biogeographic features: central Victoria (e.g. Yarra and Dandenong Ranges), the
Australian Alps, the Hunter River valley, and the Border Ranges. The phylogeographic
structure of this fauna indicates that these patterns are very old and their origins pre-
date widespread aridification during the Neogene. Relationships amongst species
found in Victoria and into South Australia are poorly defined, suggesting an ancient
relict fauna that is the outcome of major extinction events.
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The southwestern fauna is relictual and much less diverse: nine species that evolved
during drastic climate changes in the Middle Miocene from warm and wet to
permanently cooler and drier conditions. This fauna is restricted to climate refugia in
mountain ranges and wet forests. Fragmented contemporary distributions and high
genetic partitioning within species suggests localised long-term persistence and
extensive past extinction. Future distribution modelling indicates that this restriction
may facilitate survival in a forthcoming period of anthropogenic warming.

At a local scale, I investigated the population structure of Pseudotyrannochthonius
giganteus endemic to mesic eucalypt forests in southwestern Australia. These forests
are a remnant of past warm/wet periods and restricted to some 8000 km2 in the
extreme southwest of Western Australia. Genetic diversity in this species is clustered in
a small region with the highest annual rainfall and lowest seasonality in Western
Australia. Distribution modelling indicates contraction towards this climate refugium
and persistence under warmer and drier future climates, assisting conservation
planning.

Taxonomic implications: as first steps to translating phylogenetic data into taxonomic
outcomes I revised the karst fauna of the Australian mainland because the majority of
currently recognised species were originally described from caves. The subterranean
fauna is not diverse: only two specialised cave dwellers. The remaining species are
epigean but had not previously been recorded from forest habitats. I also named a
pseudoscorpion in honour of Ludwig Leichardt, one of the early naturalists exploring
the Australian continent, and to pay tribute to taxonomy: the foundation of
evolutionary biology.

In this thesis I have paved the way towards an invertebrate perspective on global
biogeography, using an old but dynamic lineage exceptionally suited to infer
evolutionary history in mesic biomes. Despite the global importance of ancient
vicariance driven by continental drift and formation of major barriers, e.g. seaways and
mountain ranges, this lineage has co-evolved dynamically with its primary habitat,
mesic forests across the world. Consequently the Pseudotyrannochthoniidae have
revealed biogeographic aspects of mesic biome evolution at virtually every scale: from
extremely ancient pre-Pangaean diversifications to the ‘recent’ Quaternary colonisation
of emerging subterranean habitats in southwestern Australia.

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Table of Contents

Dedication ......................................................................................................................... v
Summary ............................................................................................................................ vii
Table of Contents ........................................................................................................... ix
Acknowledgements ...................................................................................................... xiii
Thesis Declaration ......................................................................................................... xvii

CHAPTER ONE:
Introduction – The story begins! ....................................................................................... 0001
1.1 Biogeography ....................................................................................................... 0003
1.2 Mesic habitats across the world ........................................................................ 0004
1.3 Arachnids and their contribution to biogeography ....................................... 0005
1.4 The pseudoscorpion family Pseudotyrannochthoniidae .............................. 0006
1.5 The Australian fauna of Pseudotyrannochthoniidae ..................................... 0008
1.6 Mesic habitats in Australia ................................................................................. 0009
1.7 Research aims and thesis structure ................................................................... 0010
1.8 Remarks on thesis style ...................................................................................... 0014

CHAPTER TWO:
Biogeography of Pangaea: insights from a globally distributed lineage of pseudo-
scorpions from temperate biomes .................................................................................... 0017
2.1 Abstract ................................................................................................................. 0019
2.2 Introduction .......................................................................................................... 0020
2.3 Materials and methods ....................................................................................... 0022
2.4 Results ................................................................................................................... 0031
2.5 Discussion ............................................................................................................. 0039
2.6 Conclusions .......................................................................................................... 0046
2.7 Acknowledgements ............................................................................................ 0047
2.8 Supporting information ...................................................................................... 0048

CHAPTER THREE:
Phylogeography of Australian mesic biota: diversity and distributions in an ancient
arachnid lineage showcase the importance of temperate refuges .............................. 0075
3.1 Abstract ................................................................................................................. 0077
3.2 Introduction .......................................................................................................... 0078
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3.3 Materials and methods ........................................................................................ 0080
3.4 Results .................................................................................................................... 0090
3.5 Discussion ............................................................................................................. 0097
3.6 Acknowledgements ............................................................................................. 0105
3.7 Supporting information ...................................................................................... 0106

CHAPTER FOUR:
On gaps and gradients: climatic history and geology shape phylogeographic
structure in a widespread arachnid lineage (Pseudoscorpiones: Pseudotyranno-
chthoniidae) from mesic eastern Australia ..................................................................... 0129
4.1 Abstract ................................................................................................................. 0131
4.2 Introduction .......................................................................................................... 0133
4.3 Materials and methods ........................................................................................ 0136
4.4 Results .................................................................................................................... 0143
4.5 Discussion ............................................................................................................. 0149
4.6 Acknowledgements ............................................................................................. 0158
4.7 Supporting information ...................................................................................... 0159

CHAPTER FIVE:
Climate change coincides with diversification in a biodiversity hotspot: phylogeo-
graphy of ancient pseudoscorpions in southwestern Australia .................................. 0173
5.1 Abstract ................................................................................................................. 0175
5.2 Introduction .......................................................................................................... 0176
5.3 Materials and methods ........................................................................................ 0177
5.4 Results .................................................................................................................... 0185
5.5 Discussion ............................................................................................................. 0194
5.6 Acknowledgements ............................................................................................. 0198
5.7 Supporting information ...................................................................................... 0200

CHAPTER SIX:
The origins of diversity in ancient landscapes: deep phylogeographic structuring in
a pseudoscorpion (Pseudotyrannochthonius) reflects Plio-Pleistocene
climate fluctuations ............................................................................................................. 0215
6.1 Abstract ................................................................................................................. 0217
6.2 Introduction .......................................................................................................... 0218
6.3 Materials and methods ........................................................................................ 0220
6.4 Results .................................................................................................................... 0224
6.5 Discussion ............................................................................................................. 0229
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