The evolution of terrestrial breeding in African amphibians

197 Pages·2014·24.23 MB·English

by  Christoph Liedtke

T E T
HE VOLUTION OF ERRESTRIAL
B A A
REEDING IN FRICAN MPHIBIANS

Inauguraldissertation
zur
Erlangung der Würde eines Doktors der Philosophie
vorgelegt der
Philosophisch-Naturwissenschaftlichen Fakultät
der Universität Basel
von

Hans Christoph Liedtke
aus Deutschland

Basel, 2014
Genehmigt von der Philosophisch-Naturwissenschaftlichen Fakultät
auf Antrag von

Prof. Dr. Peter Nagel (Fakultätsverantwortlicher)

PD Dr. Simon P. Loader (Dissertationsleiter)
Dr. Ivan Gomez-Mestre (Korreferent)

Basel, den 24. Juni 2014

Prof. Dr. Jörg Schibler (Dekan)

T C
ABLE OF ONTENTS

Introduction 1
Adaptation, life history and the comparative method 2
Amphibian life history and terrestrial breeding 4
Continental Africa 7
Objectives 9
Chapter overview 10
References 12
Chapter I 15
Forest as Promoters of Terrestrial Life-History Strategies in East African Amphibians 16
Chapter II 21
Interspecific Patterns for Egg and Clutch Sizes of African Bufonidae (Amphibia: Anura) 22
Supplement: Phylogenetic Non-Independence of Trait Data 29
Chapter III 36
No Ecological Opportunity on a Continental Scale? Diversification and Life-History
Evolution of African True Toads (Bufonidae: Anura) 37
Chapter IV 70
Evolution of Viviparity in African Anurans 71
Synthesis 94
Discussion 95
Caveats 100
Future Directions 101
Conclusion 103
References 103
Acknowledgements 106
Supplementary Materials
Chapter I 108
Chapter II 125
Chapter III 130
Chapter IV 180
Curriculum Vitae 187
INTRODUCTION

I
NTRODUCTION

1
INTRODUCTION

Adaptation, life history and the comparative method

The study of adaptive traits – a trait or integrated suite of traits that increase the fitness of its
possessor (Freeman and Herron 2007) – and the related process of adaptation has long been
an important field of study for naturalists. However, it was not until Darwin and Wallace’s
theory on natural selection (Darwin & Wallace, 1858) that the concept of adaptive traits
being the product of selection was understood and after which point the terms ‘adaptation’
and ‘evolution’ became almost interchangeable (but see e.g. Harvey and Pagel 1991; Stearns
1992 for discussion on different uses of the term). Adaptation as a response to environmental
change is deeply embedded in biological theory (Dobzhansky 1950a; 1950b), but this
interaction has historically been interpreted in a number of different ways. Lamarck for
example, suggested that changes in an organism’s immediate environment brought about
‘adaptive traits’ in the organism that better suit its environment, traits that are then passed on
to the next generation (Futuyma 1998). In contrast, Darwin and Wallace proposed that the
organism itself does not change in any significant (or heritable) way, but that population
variation and changes in the environment (abiotic and biotic) shifts the probabilities for
survival and reproductive success, thereby providing a mechanism for adaptive change over
generations.
With the rediscovery of Mendel’s law of inheritance in 1900 and developments in the
field of genetics (Dobzhansky 1950c), the ‘modern synthesis’ of evolutionary theory could
establish the relationship between two fundamental components of a trait: the genotype and
the phenotype (Stearns 2000). The genotype (the inherited genetic information) allows for
hereditable variability to persist and be passed on in a population, and the phenotype, the
manifestation of the genotype in a given environment and developmental conditions, exhibits
traits of different fitness upon which selection then acts. The study of the evolution of fitness
components related to the life-cycle of an organism has forged the discipline of life history
evolution (Stearns 1992).
One of the longstanding interests in life history evolution, in fact biology as a whole, has
been to explain the remarkable diversity of reproductive strategies on earth. A reproductive
strategy is a complex of interrelated life history components such as age at maturity, fecundity
and length of life, and to understand the variation in these traits, studies have traditionally
2
INTRODUCTION
adopted an optimality approach that has become known as the ‘life history theory’. This
theory predicts that natural selection acts to maximize an individual’s inclusive fitness in a
given environment, given underlying intrinsic (e.g. genetic) constraints (Stearns 2000). This
foundation has lead to hallmark studies in ecology (e.g. Lack 1947; MacArthur and Wilson
1967) and has benefitted hugely from more recent inclusions of reaction norms and frequency
and density dependent selection models (Stearns 2000). However, the optimality model is
somewhat restricted to within-lineage variations and local adaptations, and less suited for
studying how lineage-specific traits differ, at which taxonomic level differences occur and how
they might have evolved (Stearns 1992). It is at this stage where life history evolution and
comparative biology intersect.
Comparative biology uses comparisons of a variable (e.g. trait states, speciation rates,
environmental conditions etc.) across a range of taxa to pose or test hypotheses on adaptation
and other evolutionary processes (Futuyma 1998). For example, moving from marine to
brackish and fresh water habitat has repeatedly resulted in increased egg size, decreased
fecundity and abbreviated larval development in independent decapod lineages (Diesel et al.
2000), long-distance migration is likely to have played a key role in the origin of semelparity
in various species of pacific salmon (Crespi and Teo 2002) and tropical birds have a slower
pace of life than temperate birds (Wiersma et al. 2007). Although simple in its premise, some
authors go so far as to say that ‘comparative studies have taught us most of what we know
about adaptation’ (preface in Harvey and Pagel 1991). Before the popularization of
integrating phylogenetic trees with comparative methods, comparative biology was largely
restricted to non-directional studies where comparisons were made only across taxa at similar
phylogenetic levels. Directional studies opened the door to estimating ancestral states and
detecting correlated, parallel or convergent evolution (Harvey and Pagel 1991). Far more
importantly, the inclusion of a phylogeny quantifies the degree of independence of an
evolutionary occurrence, a fundamental assumption in comparative biology that was largely
ignored for a long time (Felsenstein 1985). These advancements in comparative phylogenetic
methods are making it increasingly possible to quantitatively study aspects of life history
evolution, adaptation to changes in the environment and the implications these adaptations
may have on the diversification and evolutionary success of lineages.
Using African amphibians as model taxa, this thesis investigates the evolution of life
history strategies, how these may be evolutionarily correlated with the environment and

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INTRODUCTION
whether more terrestrial modes of reproduction may have favoured the diversification of
lineages on a historically dry continent.

Amphibian life history and terrestrial breeding

Amphibians are tetrapod vertebrates that derived from osteolepiform fish in the Devonian, ca.
400 million years ago (Carroll 2001) and their life cycle are usually ‘biphasic’, consisting of an
aquatic larval stage and a terrestrial adult stage. There are currently just over 7200 described,
extant species of amphibians (Frost 2014) belonging to three orders: Anura (ca. 6350 species),
Caudata (ca. 670 species) and Gymnophiona (ca.
200 species). Together, these make up the
Lissamphibia (Figure 1). Anurans – frogs and
toads – are the most wide spread group with a
near global distribution, whereas caudates –
salamanders and newts – are more or less
restricted to the northern hemisphere (with
recent immigration into northern South
America; Elmer et al. 2013). Gymnophiona –
the caecilians – are restricted to the tropics. How
these three orders are related to each other and
the monophyly of Lissamphibia has long been
debated (summarized in Duellman and Trueb
FIGURE 1. The phylogenetic relationship of
lissamphibia based on the ‘batrachian 1994), but there is a growing body of evidence in
hypothesis’ and their distributions.
favour of the ‘Batrachia hypothesis’ (San Mauro
et al. 2004; 2005; Roelants et al. 2007; San Mauro 2010) that places Gymnophiona as the
sister lineage to Batrachia (Anuran + Caudata; Figure 1). Based on their distribution, it was
traditionally thought that vicariance, caused by the breakup of Pangaea (Feller and Hedges
1998), was the likely process of cladogenesis among the main amphibian groups. However
many of the amphibian lineages predate Pangaea fragmentation and so ecological
specialization has been suggested as a plausible alternative (San Mauro et al. 2005).
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