Download Sexual selection and speciation

Sexual selection and speciation:
Mechanisms in Lake Victoria cichlid fish
PhD Thesis of Martine Maan
Universiteit Leiden
Defence May 11th 2006
SUMMARY
Aims and Scope
In this thesis, I investigate the selective forces acting on colour traits and mate
preferences for these traits in Lake Victoria cichlid fish. The rationale behind this
objective is as follows: whereas it is increasingly appreciated that the tremendous
colour variation among haplochromine cichlids plays an important role in both
inter- and intraspecific mate choice, very little is known about the processes that
drive (or constrain) the evolution of these colour signals and colour preferences in
the first place. Sexual signalling may be subject to a variety of evolutionary
pressures, exerting selection on both the senders and receivers of sexual signals.
Insight in these selection pressures is required to assess the importance of
haplochromine colours for the evolution of their extraordinary diversity.
I focus on two representative model systems: a pair of sibling species in the
genus Pundamilia (Chapters 2-6) and the highly polymorphic species Neochromis
omnicaeruleus (Chapters 7-8). In both laboratory and field conditions, I investigate
the nature and strength of several possible determinants of haplochromine colour
signalling. I evaluate the consequences of my findings for the hypothesis that sexual
selection by mate choice contributes to haplochromine speciation.
Summary of the Chapters
Chapters 2-6: blue and red: the divergence of Pundamilia pundamilia and
Pundamilia nyererei
Pundamilia pundamilia (Seehausen et al. 1998a) and P. nyererei (Witte-Maas & Witte
1985) are two very closely related species of Lake Victoria cichlids, that form
reproductively isolated and ecologically differentiated sympatric sister species in
some localities, but interbreeding colour morphs or incipient species in other
localities. They represent a common pattern of colour variation among Lake
Victoria haplochromine cichlids (Seehausen et al. 1999c). Pundamilia pundamilia
males are metallic grey-blue and Pundamilia nyererei males are yellow laterally and
bright red dorsally (see Figure 5.1, page 81). The two species are morphologically
similar; the cryptically coloured females can be distinguished only with difficulty.
Where water clarity permits colour signal transduction, the two species are
differentiated, females have species-assortative mating preferences and use male
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coloration as a choice criterion (Seehausen & Van Alphen 1998). Within P. nyererei,
male coloration is a more extreme red where water clarity and hence signal
transduction is better. These observations lead to the hypothesis that sexual
selection has been a driving force in the divergence of this species pair. This
scenario rests on the premise that the phenotypic traits responsible for reproductive
isolation between sister species evolve under sexual selection within species.
However, interspecific differences in characters subject to mate choice do not
necessarily signify that sexual selection was the cause of their divergence (Lande
1981; West-Eberhard 1983; Boake 2002). In Chapter 2, I tested this premise in
Pundamilia nyererei. I studied a population at Makobe Island in the western Speke
Gulf (Seehausen & Bouton 1997; Figure 6.1 on page 93), where the water is
relatively clear. I carried out behavioural mate-choice experiments in the laboratory,
field observations on territorial males in the lake, and a mesocosm experiment
under semi-natural conditions, in which actual mating occurred. I found that male
red coloration is subject to directional sexual selection by female mate choice: in
both laboratory and field conditions, females responded more frequently to the
courtship displays of brighter red males than to those of less bright males. This is
consistent with the hypothesis that intraspecific sexual selection through female
choice has driven the divergence in male coloration between P. nyererei and P.
pundamilia. I also found that male territoriality is vital for male reproductive success,
and that females tend to mate with more than one male for the fertilisation of a
single clutch of eggs.
In Chapters 3 and 4, I investigated whether female preferences in Pundamilia
may be driven by selection for ‘good genes’, and I assessed the potential for this
selection to contribute to the divergence of P. pundamilia and P. nyererei. First
(Chapter 3) I studied fitness correlates of male coloration in Pundamilia nyererei. As
demonstrated in Chapter 2, male red coloration in this species is subject to
intraspecific sexual selection by female mate choice. Here, in the same field
population, I found that variation in the extent and brightness of male coloration
elements was not associated with variation in a set of strongly interrelated indicators
of male dominance: male size, territory size and territory location. Instead, male
territory size and coloration were independent predictors of male quality: female
preferences for bright red males and males with large territories both selected
against heavily parasitized males. Consistent with parasite-mediated sexual selection
(Hamilton & Zuk 1982), males had higher and more variable parasite loads than
females. I also showed that male coloration is carotenoid-based, illustrating the
potential for honest signalling: carotenoids, while probably a limiting resource, are
necessary for a variety of beneficial physiological functions, particularly in immune
defence (Olson & Owens 1998; Hill 1999). Consequently, carotenoid displays are
physiologically costly to produce and maintain, and thereby fulfil the requirements
of an honest signal of individual quality (Zahavi 1975; Lozano 1994).
To investigate whether parasite-mediated sexual selection might have
contributed to the divergence of female mating preferences and male colours
between P. pundamilia and P. nyererei, I also studied the relationship between male
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nuptial coloration and parasite load in P. pundamilia from Makobe Island (Chapter
4). As described above, P. pundamilia males have metallic grey-blue bodies and
dorsal fins, but their anal and caudal fins can be bright red. I found that this red
coloration of P. pundamilia fins seems to be chemically similar to that in the body and
fins of P. nyererei, but that it is not significantly associated with parasite load. Instead,
I found that the blue coloration on the body and dorsal fin is negatively correlated
with parasite load. I also found that parasite infestation rates differ quantitatively
between the species, in a way that is consistent with species differences in diet and
microhabitat. These results suggest that at an island where the sister species are
genetically and ecologically well differentiated, parasite-mediated sexual selection
within each species could cause divergent selection between the species on male
coloration and parasite resistance. Hence, divergent sexual selection may not be
inconsistent with ‘good genes’ models of sexual selection. I conclude that in
populations where P. pundamilia and P. nyererei are ecologically differentiated,
parasite-mediated sexual selection may strengthen reproductive isolation between
the two species.
Divergent parasite-mediated sexual selection may not be enough to drive
species divergence. This is because intermediate phenotypes are likely to experience
intermediate parasite exposure rates and may therefore do well in intermediate
habitats. As a result, assortative mating will not evolve. In Chapter 5, I therefore
investigated another mechanism, that could have driven the divergent evolution of
male coloration and female mating preferences between P. pundamilia and P.
nyererei: divergent sensory drive. Several recent studies have presented evidence for
divergent sensory drive in species that use visual signals in sexual communication
(Boughman 2001; Fuller 2002; Leal & Fleishman 2004), indicating that it may be a
potent driving force in speciation (Endler & McLellan 1988; Boughman 2002). The
hypothesis that sensory drive has been involved in the divergence of P. pundamilia
and P. nyererei (Seehausen et al. 1997a) predicts that i) the photic environment in
the microhabitat of the two species differs, ii) visual systems of the two species have
diverged in adaptation to these different photic environments, and that iii) within a
species, females prefer more conspicuous over less conspicuous males. As
demonstrated in Chapter 2, the latter is the case for at least one of the two species:
the red coloration of P. nyererei males is subject to directional sexual selection by
female choice and the extent and brightness of red is negatively correlated with
parasite load (Chapter 3). As demonstrated in Chapter 4, the extent of blue
coloration in P. pundamilia males is negatively correlated with parasite load too.
Here, I quantified the light environments of P. pundamilia and P. nyererei at Makobe
Island and I demonstrated that they differ significantly: P. nyererei, which breeds in
deeper water than P. pundamilia, inhabits a more red-shifted habitat. Whereas P.
nyererei and P. pundamilia differ in visual properties at the molecular level (Carleton
et al. 2005), it was unknown whether these species also differ in the perception of
red and blue stimuli, in a way that could explain the divergent mating preferences
of the two species. I used the optomotor response test to measure the contextindependent behavioural responses to coloured light in both species. I found that
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the species differ in the predicted direction: P. pundamilia is more sensitive to blue
light and P. nyererei is more sensitive to red light. I conclude that divergent sensory
drive in a heterogeneous environment may have driven the divergence of P.
pundamilia and P. nyererei. The fully sympatric distribution of the two species
suggests that this process occurred without geographical isolation. Currently, the
potentially isolating effects of parasite-mediated sexual selection for bright colours
(Chapters 3 and 4) could further contribute to the maintenance of reproductive
isolation between P. pundamilia and P. nyererei.
Over the last decades, water transparency in Lake Victoria has been declining
(Verschuren et al. 2002). Because many haplochromine cichlids rely on visual cues
for mate recognition (Seehausen & Van Alphen 1998; Knight & Turner 2004),
increased turbidity poses a threat to species diversity because it affects the rate of
hybridisation between closely related species (Seehausen et al. 1997a). Also P.
pundamilia and P. nyererei increasingly hybridise as water transparency decreases,
and in extremely turbid water, single populations of slightly variable coloration are
found (Seehausen 1997). Given that interspecific mate choice is affected by water
transparency, the nature and strength of sexual selection on male coloration within
species may be affected too. Indeed, across populations of P. nyererei, water
transparency and the intensity of male coloration are correlated (Seehausen et al.
1997a). However, two different mechanisms may account for this relationship: i)
female mating preferences and male colour may co-evolve in response to variation
in water transparency, or ii) the strength of selection on male coloration by female
mating preferences may be a function of signal transduction through the water,
without mating preferences evolving themselves. I investigated these alternatives in
Chapter 6. I studied the mate choice behaviour of a P. nyererei population from
turbid water, and I used the same laboratory set-up as in Chapter 2 to allow for
comparison of the clear and the turbid water populations. I found that in the
population from turbid water, female preference for male red coloration is
significantly weaker than in the population from clear water. I also found that both
the amount and the hue of male red coloration differ significantly between
populations, consistent with adaptation to the different photic habitats of the two
populations. These findings suggest that the observed correlation between male
coloration and water transparency is not mediated by environmental variation
alone. Rather, they indicate that female mating preferences have evolved in
response to this variation. This is the first evidence for intraspecific preference-trait
co-evolution in cichlid fish, confirming the earlier suggestion that the decrease in
Lake Victoria water transparency affects both interspecific mate choice and
intraspecific sexual selection (Seehausen et al. 1997a). This underlines the
importance of measures to counteract the ongoing eutrophication of Lake Victoria.
Chapters 7-8: the colour morphs of Neochromis omnicaeruleus
By definition, speciation by sexual selection requires variation in mate preferences
and preferred traits within species. Neochromis omnicaeruleus is a suitable model
system to study such intraspecific variation, because it is one of the most
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SUMMARY
polychromatic haplochromines known (Seehausen 1996). In addition to the blotch
polymorphism which is the subject of Chapter 8, there is considerable colour
variation among the individuals belonging to the presumably ancestral, not-blotched
phenotype: male coloration ranges from sky-blue to yellow-red and females are
grey-blue to yellow (see Figure 7.1 on page 113).
In Chapter 7, I present the first investigation of the blue/yellow
polychromatism of N. omnicaeruleus. In a wild population at Makobe Island, I found
that male colour is associated with size and sexual maturity: yellow males are smaller
than blue males and tend to be sexually immature. In females, size and maturity do
not differ between colour types. Laboratory crosses revealed that there is a heritable
component to the observed colour variation: yellow parents produced more yellow
offspring than blue parents. Together with repeated aquarium observations of
yellow individuals that gradually become blue, these data suggest that yellow males
change to blue as they approach sexual maturity, and that the occurrence and
timing of this transition is influenced by both environmental and genetic effects.
Importantly, some males mature and may start breeding while they are still yellow.
Because haplochromine colour patterns mediate inter- and intraspecific mate choice
(Seehausen & Van Alphen 1998; Seehausen et al. 1999b; Knight & Turner 2004;
this thesis), the blue-yellow polychromatism of N. omnicaeruleus might serve as a
target for diversifying sexual selection and provide a starting point for species
divergence. Indeed, this polychromatism resembles the colour variation present
among sister species of other haplochromine cichlids (Florin 1991; Seehausen et al.
1999c).
In addition to the blue-yellow phenotypes, two types of blotched morphs
occur in both sexes of N. omnicaeruleus: orange-blotched and white-blotched (Figure
8.4 on page 128). Similar blotch colour polymorphisms are observed in several East
African haplochromine cichlids, often associated with sex reversal genes. In N.
omnicaeruleus, blotch-linked dominant female determiners can be compensated by
autosomal male rescue genes, required to create blotched males. These associations
and interactions between sex and colour genes generate selection favouring matings
between matching genotypes that yield even offspring sex ratios. Therefore, blotch
polymorphisms and sex determination genes may play an important role in the
evolution of haplochromine species diversity (Lande et al. 2001). In N. omnicaeruleus,
matings between blotched phenotypes and those plain phenotypes that do not
possess rescue genes yield distorted offspring sex ratios. Most colour-sex
combinations exert mating preferences that would avoid this, but blotched females
do not exert any preferences (Seehausen et al. 1999b). Possibly, the spread of
assortative mating preference genes in blotched females is precluded by the
extremely low abundance of blotched males in the population studied: whereas
about half of all females is blotched, 99% of the males has the plain phenotype. Since
laboratory experiments on the genetics of the system suggested that blotched males
should not be uncommon, and because the blotched colour pattern seems very
conspicuous, Seehausen et al. (1999b) hypothesised that blotched fish may suffer
increased predation from visual hunters. This idea is investigated in Chapter 8. In a
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predation experiment using wild kingfishers, I found that blotched fish indeed
incur more predator attacks. Under water observations in the lake further suggested
that sexual dimorphism in behaviour may account for an additional risk for males. A
population census however showed that blotched males are rare already as juveniles.
Yet, female phenotype frequencies were inconsistent with disassortative mating that
could account for a lower production of blotched males. Therefore, to explain the
scarcity of blotched males in nature there should be selection against blotched males
early in life. Alternatively, the genetic architecture underlying the phenotypic
distribution of colour and sex is more complex than the minimum model deduced
from laboratory crosses. In fact, my results emphasise the need for extensive study
of the underlying genetics.
Whereas my study does not provide a conclusive explanation for the
dynamics of the Neochromis omnicaeruleus blotch polymorphism, it does suggest that
differential predation with regard to colour pattern and possibly sex, is an
important selective force in the evolution and maintenance of mating preferences
and colour gene expression. As such, my results indicate that natural selection by
visual predators may hinder the establishment of conspicuous colour morphs in
haplochromine cichlid fish. This may hold for other sexually selected colour
patterns in haplochromine cichlids too. Thereby, predation may set a limit on the
exaggeration of sexually selected traits and increase the potential for honest
signalling.
Chapter 9: Synthesis
In the final Chapter, I summarise the main findings of the work presented in this
thesis. I conclude that the evolution of haplochromine colour patterns is subject to
several simultaneous selection pressures. First, I found evidence for directional
sexual selection for male quality. Second, my work indicates that habitat
heterogeneity, in terms of photic environment and parasite exposure, may promote
population divergence in male nuptial coloration and female preferences.
Consequently, I argue that sexual selection need not be ‘Fisherian’ in order to
become divergent. Third, I found that predation pressure and water turbidity may
constrain the evolution and persistence of conspicuously coloured morphs and
species.
Together, these selection pressures and their interactions determine local
species diversity. I discuss the implications of my findings for our understanding of
haplochromine speciation, and I briefly indicate how my results may affect the
direction of future work.
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