Evolution of Colony Characteristics in The Harvester Ant Genus

217 Pages·2005·6.03 MB·English

Evolution of Colony
Characteristics in
The Harvester Ant Genus
Pogonomyrmex

Dissertation zur Erlangung des naturwissenschaftlichen Doktorgrades der
Bayerischen Julius-Maximilians-Universität Würzburg

vorgelegt von
Christoph Strehl
Nürnberg

Würzburg 2005
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Eingereicht am: .........................................................................................................

Mitglieder der Prüfungskommission:
Vorsitzender: .............................................................................................................
Gutachter : .................................................................................................................
Gutachter : .................................................................................................................

Tag des Promotionskolloquiums: ..............................................................................
Doktorurkunde ausgehändigt am: .............................................................................
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1. Index
1. Index.................................................................................................................5
2. General Introduction and Thesis Outline.......................................................7
1.1 The characteristics of an ant colony......................................................8
1.2 Relatedness as a major component driving the evolution of colony
characteristics.................................................................................................10
1.3 The evolution of polyandry: ultimate and proximate causes................11
1.4 Polygyny and slavery..........................................................................13
1.5 Morphological polymorphisms between workers and queens..............14
1.6 Introduction to the study genus Pogonomyrmex..................................16
1.7 Outline of the thesis............................................................................26
1.8 Publications........................................................................................28
1.9 Literature............................................................................................28
3. Determinants of Intracolonial Relatedness in Pogonomyrmex rugosus
(Hymenoptera; Formicidae): Mating Frequency and Brood Raids....................41
3.1 Abstract..............................................................................................41
3.2 Introduction........................................................................................41
3.3 Materials and methods........................................................................43
3.4 Results................................................................................................46
3.5 Discussion..........................................................................................48
3.6 Acknowledgements.............................................................................53
3.7 Tables.................................................................................................53
3.8 Figures................................................................................................57
3.9 References..........................................................................................58
4. Extremely High Mating Frequency in the Florida Harvester Ant
(Pogonomyrmex badius).........................................................................................62
4.1 Abstract..............................................................................................62
4.2 Introduction........................................................................................62
4.3 Methods..............................................................................................66
4.4 Results................................................................................................70
4.5 Discussion..........................................................................................72
4.6 Acknowledgements.............................................................................76
4.7 Appendix............................................................................................77
4.8 References..........................................................................................88
5. A Genetic Component in the Determination of Worker Polymorphism in
the Florida Harvester ant Pogonomyrmex badius................................................92
5.1 Summary............................................................................................92
5.2 Introduction........................................................................................92
5.3 Methods..............................................................................................94
5.4 Results................................................................................................95
5.5 Discussion..........................................................................................95
5.6 Acknowledgments..............................................................................97
5.7 References..........................................................................................97
5.8 Tables.................................................................................................99
6. Cladistic Analysis of Paleo-Island Populations of the Florida Harvester
Ant (Hymenoptera: Formicidae) Based Upon Divergence of Mitochondrial
DNA Sequences....................................................................................................103
6.1 Abstract............................................................................................103
6.2 Resumen...........................................................................................103
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6.3 Introduction......................................................................................104
6.4 Materials and Methods......................................................................105
6.5 Results..............................................................................................109
6.6 Discussion........................................................................................113
6.7 Acknowledgments............................................................................114
6.8 References cited................................................................................115
7. Colony structure and morphometrics in the queen dimorphic harvester
ant, Pogonomyrmex pima.....................................................................................118
7.1 Summary..........................................................................................118
7.2 Introduction......................................................................................118
7.3 Methods............................................................................................120
7.4 Results..............................................................................................122
7.5 Discussion........................................................................................125
7.6 Acknowledgments............................................................................129
7.7 References........................................................................................130
7.8 Table.................................................................................................133
7.9 Figures..............................................................................................135
8. Colony Structure and Sociogenetics of the Queen Dimorphic Harvester
Ant, Pogonomyrmex (Ephebomyrmex) pima.......................................................137
8.1 Abstract............................................................................................137
8.2 Introduction......................................................................................137
8.3 Materials and Methods......................................................................140
8.4 Results..............................................................................................144
8.5 Discussion........................................................................................147
8.6 Acknowledgements...........................................................................153
8.7 Tables...............................................................................................154
8.8 Figures..............................................................................................158
8.9 References........................................................................................159
9. Phylogeny of the Harvester Ant Genus Pogonomyrmex (Hymenoptera:
Formicidae) in North-America and its relation to South-American
Pogonomyrmex species........................................................................................165
9.1 Abstract............................................................................................165
9.2 Introduction......................................................................................165
9.3 Material and Methods.......................................................................168
9.4 Results..............................................................................................170
9.5 Discussion........................................................................................174
9.6 Acknowledgments............................................................................177
9.7 Figures..............................................................................................178
9.8 Tables...............................................................................................185
9.9 Literature..........................................................................................191
10. General Discussion......................................................................................196
11. Summary......................................................................................................207
12. Zusammenfassung.......................................................................................209
13. Curriculum Vitae.........................................................................................212
14. Publikationsliste...........................................................................................214
15. Danksagung.................................................................................................216
16. Ehrenwörtliche Erklärung..........................................................................217
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2. General Introduction and Thesis Outline

“For such is the way of it: to find and lose, as it seems to
those whose boat is on the running stream”
(Tolkien 1991, p.399)

The selective forces of evolution created a manifold life with impressive forms in
shaping not only the morphology of species, but also their behavior. An extraordinary
example for the evolution of behavioral characters is the clumping of individuals into
one single group that collectively performs social tasks. Its apex is an altruistic self
restraint, as found in impressive ways among colonies of ants or bees (eusocial
Hymenoptera): their eusocial colonies are not only characterized by overlapping
generations and cooperative brood care by the adults, but also by a reproductive
division of labor implementing the presence of non-reproductive helpers as “workers”
(Michener 1969; Wilson 1971; Alexander 1974; Michener 1974; Hölldobler and Wilson
1990; Ratnieks and Anderson 1999).
The altruistic behavior of eusocial Hymenoptera was for a long time explained by the
perception of natural selection not only acting at the level of single organisms, but also
at the family-level (Darwin 1859). Later, this was mathematically formulated by
Hamilton in his theory of kin selection (Hamilton 1964), which is now the key concept
for explaining the evolution of group living behavior. The Hymenopteran sex
determination system hits the underlying genetic assumption of Hamilton’s formula (br-
c>0; b = benefits connected to behavior, r = relatedness of actor to recipient, c = costs
involved for actor), because unfertilized eggs become males and fertilized eggs
normally females (relatedness “asymmetry”) (Hamilton 1964; Trivers and Hare 1976).
By this the cost to benefit ratio for ‘altruistic’ behaviors decreases for females, favoring
their accumulation in eusocial groups (colonies).
Group living is quite divers, and might even be lost again if no longer favorable,
depending on internal and external needs (Heinsohn and Legge 1999; Gadagkar 2002;
Krieger and Ross 2002; Roux and Korb 2004). Basic rules generating these social
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phenotypes are pertinent across taxa, and they produce ubiquitous patterns of social
organization, like mass action responses, division of labor and social hierarchies (Fewell
2003). The tremendous variety of group living among Hymenoptera (bees, ants, wasps)
has its greatest diversity among ants (Formicidae), making them especially suitable in
studying the characteristics of social colonies (Hölldobler and Wilson 1990).
In the present work analyses on the evolution of colony characteristic in the harvester
ant genus Pogonomyrmex (Hymenoptera: Formicidae) will be presented and discussed.
In the following chapters of this introduction in a first step the general characteristics of
an ant colony will be described, relatedness as a major component driving the evolution
of colony characteristics is introduced, and the phenomena of polyandry, polygyny and
morphological polymorphism are emphasized. Subsequently the studied genus
Pogonomyrmex and the aims of this study are introduced.
1.1 The characteristics of an ant colony
Several characters are prominent in constituting ant-colonies (e.g.: Alexander 1974;
Gordon 1984b; Hölldobler and Wilson 1990; Gordon 1995; Ratnieks and Anderson
1999; Sanders and Gordon 2000; Anderson and McShea 2001; Fewell 2003): (1)
number of individuals (colony size); (2) cohesion (nest, odor, age); (3) nest architecture;
(4) organization of colony members (e.g. reproductive division of labor, task allocation,
information transfer); (5) robustness (e.g. defense, disease and parasite transmissibility,
territoriality in space and time); (6) efficiency (e.g. resource use, reproductive output);
(7) relatedness among colony members.
These single colony characteristics are influenced by various factors. For illustration,
task performance and division of labor, which constitute a wide field of recent research,
are effected among other things by colony size (Murakami et al. 2000; Gautrais et al.
2002), circadian rhythmic (Gordon 2002; Wuellner and Saunders 2003), information
transfer (Gordon 1989; Tofts and Franks 1992; Franks et al. 2001; Fewell 2003),
presence or absence of queens (Vienne et al. 1998; Backen et al. 2000; Heinze and
Keller 2000; Kikuchi and Higashi 2001), or genetic variability (Stuart and Page 1991;
Myerscough and Oldroyd 2004). Analogous several other factors exist, which influence
group living behavior in ants.
In the main, colony characteristics are influenced by extrinsic environmental and
intrinsic nest factors (e.g.: Alexander 1974; Fewell 2003). For example changes of the
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external environment are influencing the colonies efficiency and robustness, and can be
managed via a flexible response of the whole colony, e.g. by information transfer in the
“social environment” between colony members (Fewell 2003). Territoriality on the
other hand, i.e. the ability of colonies to obtain and maintain a certain foraging area
within their population, is strongly shaped by several intrinsic factors like behavior,
aggressiveness, or growth rate of colonies (Hölldobler 1974; Hölldobler 1979; Cole and
Wiernasz 1999; Cole et al. 2001).
Additionally single colony characteristics can be reciprocally influenced by others.
For example, pathogen resistance as important intrinsic factor is shaped by the colonies
efficiency and organization, because it is most importantly influenced by the cleanliness
of the whole colony (maybe improved by task specialists), or by the recognition of
medically parasitized individuals and their exclusion / elimination or their cure of
parasitation (Moore 1995; Julian and Cahan 1999; Bot et al. 2001; Hart and Ratnieks
2001; Moore 2002).
The benefits of group living are various and general items for the benefits of group
living, which might also be applicable to a social colony might be (1) a lowered
susceptibility to predation, e.g. via an aggressive group defense or using the group as
cover, and (2) reaching a profitable utilization of food sources, e.g. if these are scattered
(Alexander 1974). Therefore, the robustness and efficiency of ant colonies might be
regarded as being predominantly in the focus of natural selection. Particularly, the
efficient mechanisms of division of labor, “in particular series-parallel operation and
transfer of information among group members” are enabling ant colonies to interact
with an unpredictable environment (Krieger et al. 2000). These direct benefits are also
mirrored in non-Hymenopteran societies, and even robotic systems can be enhanced by
implementing such “ant-inspired algorithms” (Krieger et al. 2000).
However, “there is no automatic or universal benefit from group living” (Alexander
1974) and there are also costs involved to living in a colony (Heinsohn and Legge
1999). For example social parasitism evolved several times in ants to exploit existing
colonies (Hölldobler and Wilson 1990; Parker and Rissing 2002; Savolainen and
Vepsalainen 2003). Accordingly, the spread of medical parasites and pathogens might
be favored in eusocial groups, especially under the condition of high genetic uniformity
due to a high relatedness among group members, like in ants or bees. Additionally,
colony characteristics by themselves can have negative feedback (Fewell 2003; Johnson
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2003). For instance, there is a relationship between group size and efficiency, such that
the benefits of group living decrease in larger groups, most probably because of
interference during foraging (Krieger et al. 2000).
1.2 Relatedness as a major component driving the evolution of colony
characteristics
Although it is hard to determine characters which are applicable in explaining the
connections that occur between any two individuals within a colony, and much harder
the connections across the whole colonies society (Fewell 2003), at least the relatedness
among its members is representing such a key factor. The relatedness among its
members is influencing the various characteristics of a colony. For instance, in
Camponotus yamaokai a decrease in relatedness is affecting the cooperation of group
members, because the frequency of food exchange between workers (trophallaxis) drops
and the number of foraging workers rises (Sanada et al. 1999). Or, there might be drawn
a direct relation between colony kin structure and size (Sundström 1995; Bourke 1999),
e.g. in fungus-growing ants (Attini) where a positive correlation of mating frequency
with colony size is reported, and "some" correlation between mating frequency and
caste complexity (Murakami et al. 2000).
Relatedness is, beside costs and benefits of group living behavior, the major
component driving the evolution of colony characteristics among colony members,
according to Hamilton’s formula for kin selection (Hamilton 1964). Moreover,
nowadays relatedness measurements are easily made accessible due to the rapidly
developing molecular methods based on PCR (Saiki et al. 1985; Sambrook et al. 1989;
Simon et al. 1994; Loxdale and Lushai 1998; Hwang et al. 2001), making it a leading
tool in social insect research. Moreover, molecular markers are helping to determine
skews in the kin structure of colonies, e.g. if paternity is unequally distributed between
the mates of a queen (Boomsma and Ratnieks 1996).
Relatedness among colony members is determined by the colonies number of
matrilines, i.e. number of queens, and the number of patrilines, i.e. number of matings
per queen(s), and altered via a change in the number of matrilines and / or patrilines.
Consequently, polygyny (several queens) and multiple mating of queens (polyandry) are
main sources for genetic heterogeneity of colonies of social insects (Bourke and Franks
1995; Crozier and Pamilo 1996; Gadau et al. 1998; Heinze and Keller 2000). However,
in ants low genetic heterogeneity is caused for the most part by polygyny, whereas