Microsatellite support for active inbreeding in a cichlid fish

In wild animal populations, the degree of inbreeding differs between species and within species between populations. Because mating with kin often results in inbreeding depression, observed inbreeding is usually regarded to be caused by limited outbreeding opportunities due to demographic factors like small population size or population substructuring. However, theory predicts inclusive benefits from mating with kin, and thus part of the observed variation in inbreeding might be due to active inbreeding preferences. Although some recent studies indeed report kin mating preferences, the evidence is still highly ambiguous. Here, we investigate inbreeding in a natural population of the West African cichlid fish Pelvicachromis taeniatus which showed clear kin mating preferences in standardized laboratory experiments but no inbreeding depression. The presented microsatellite analysis reveals that the natural population has, in comparison to two reference populations, a reduced allelic diversity (A = 3) resulting in a low heterozygosity (H_o = 0.167) pointing to a highly inbred population. Furthermore, we found a significant heterozygote deficit not only at population (F_is = 0.116) but also at subpopulation level (F_is = 0.081) suggesting that inbreeding is not only a by-product of population substructuring but possibly a consequence of behavioral kin preferences.     

Heritability and adaptive significance of the number of egg-dummies in the cichlid fish Astatotilapia burtoni

Cichlid fishes are a textbook example of rapid speciation and exuberant diversity--this applies especially to haplochromines, a lineage with approximately 1800 species. Haplochromine males uniquely possess oval, bright spots on their anal fin, called 'egg-spots' or 'egg-dummies'. These are presumed to be an evolutionary key innovation that contributed to the tribe's evolutionary success. Egg-spots have been proposed to mimic the ova of the mouthbrooding females of the corresponding species, contribute to fertilization success and even facilitate species recognition. Interestingly, egg-spot number varies extensively not only between species, but also within some populations. This high degree of intraspecific variation may appear to be counterintuitive since selection might be expected to act to stabilize traits that are correlated with fitness measures. We addressed this 'paradox' experimentally, and found that in the haplochromine cichlid Astatotilapia burtoni, the number of egg-spots was related to male age, body condition and dominance status. Intriguingly, the egg-spot number also had a high heritable component (narrow sense heritability of 0.5). These results suggest that the function of egg-spots might have less to do with fertilization success or species recognition, but rather relate to mate choice and/or male-male competition, helping to explain the high variability in this important trait.     

African cichlid fish: a model system in adaptive radiation research

The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.     

Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation

Background  

Phenotypic evolution and its role in the diversification of organisms is a central topic in evolutionary biology. A neglected factor during the modern evolutionary synthesis, adaptive phenotypic plasticity, more recently attracted the attention of many evolutionary biologists and is now recognized as an important ingredient in both population persistence and diversification. The traits and directions in which an ancestral source population displays phenotypic plasticity might partly determine the trajectories in morphospace, which are accessible for an adaptive radiation, starting from the colonization of a novel environment. In the case of repeated colonizations of similar environments from the same source population this "flexible stem" hypothesis predicts similar phenotypes to arise in repeated subsequent radiations. The Midas Cichlid (Amphilophus spp.) in Nicaragua has radiated in parallel in several crater-lakes seeded by populations originating from the Nicaraguan Great Lakes. Here, we tested phenotypic plasticity in the pharyngeal jaw of Midas Cichlids. The pharyngeal jaw apparatus of cichlids, a second set of jaws functionally decoupled from the oral ones, is known to mediate ecological specialization and often differs strongly between sister-species.     

Experimental dissection of inbreeding and its adaptive significance in a flowering plant, Aquilegia canadensis (Ranunculaceae)

Inbreeding is a major component of the mating system in populations of many plants and animals, particularly hermaphroditic species. In flowering plants, inbreeding can occur through self-pollination within flowers (autogamy), self-pollination between flowers on the same plant (geitonogamy), or cross-pollination between closely related individuals (biparental inbreeding). We performed a floral emasculation experiment in 10 populations of Aquilegia canadensis (Ranunculaceae) and used allozyme markers to estimate the relative contribution of each mode of inbreeding to the mating system. We also examined how these modes of inbreeding were influenced by aspects of population structure and floral morphology and display predicted to affect the mating system. All populations engaged in substantial inbreeding. On average, only 25% of seed was produced by outcrossing (range among populations = 9-37%), which correlated positively with both population size (r = +0.61) and density (r = +0.64). Inbreeding occurred through autogamy and biparental inbreeding, and the relative contribution of each was highly variable among populations. Estimates of geitonogamy were not significantly greater than zero in any population. We detected substantial biparental inbreeding (mean = 14% of seeds, range = 4-24%) by estimating apparent selfing in emasculated plants with no opportunity for true selfing. This mode of inbreeding correlated negatively with population size (r = -0.87) and positively with canopy cover (r = +0.90), suggesting that population characteristics that increase outcross pollen transfer reduce biparental inbreeding. Autogamy was the largest component of the mating system in all populations (mean = 58%, range = 37-84%) and, as expected, was lowest in populations with the most herkogamous flowers (r = -0.59). Although autogamy provides reproductive assurance in natural populations of A. canadensis, it discounts ovules from making superior outcrossed seed. Hence, high autogamy in these populations seems disadvantageous, and therefore it is difficult to explain the extensive variation in herkogamy observed both among and especially within populations.     

Experimental evidence for adaptive phenotypic plasticity in a rock-dwelling cichlid fish from Lake Victoria

We demonstrate adaptive phenotypic plasticity (PP) in Neochromis greenwoodi , a rock-dwelling haplochromine cichlid from Lake Victoria. Adaptive phenotypic plasticity will enhance the chance of survival and reproduction in changing or novel environments. For rock-dwelling cichlids it may contribute to the success of settlement after migration between rocky outcrops or islands, since newly colonized patches of rock may offer different food regimes and different competitors. In our experiments, we simulated such situations by raising fry on different diets and with different competitors. We chose diet treatments in such a way that we could predict the direction of anatomical changes from functional demands. We expected an indirect effect of interspecific competition: selectively removing one prey-type by the competing species would leave N. greenwoodi with the other. We found the predicted phenotypic responses to food in trophic traits of N. greenwoodi . However, in the current experimental set-up we did not find a differentiating effect of species of competitor. We discuss the possible role of PP in allopatric and sympatric speciation.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 185−192.     

Wasteful carotenoid coloration and its effects on territorial behavior in a cichlid fish

The famously diverse body coloration of cichlid fish serves communicative functions in mating and social interactions including competition for resources. Here, we examined the effects of a color pattern trait—the width of a yellow bar on a black body—on territorial competition in males and females of a color variant (“Ikola”) of the Lake Tanganyika cichlid Tropheus. First, measuring integumentary carotenoid concentrations in the yellow and black body regions, we established that wider yellow bars require more carotenoids allocated to body coloration. However, we also detected high carotenoid concentrations in the black body regions (>?100 µg/g fresh skin), raising questions about the function of non-displayed integumentary carotenoids. Behavioral experiments showed that fish with wider bars were quicker to explore an unfamiliar area of the tank. In experiments including presentations of fish dummies, the bar width of ‘territorial’ dummies had no effect on the latency time which test fish took to intrude into the dummies’ territories. However, male test fish performed fewer aggressive acts against wide-barred than against narrow-barred dummy competitors. Our results suggest that intimidation by wide bars as well as correlations between bar width and explorative behavior may contribute to mediating success in territorial Tropheus “Ikola”.

     

Probing aggressive motivation in a cichlid fish

The duration of startles provides an inverse measure of motivation to resume the previous activity. Here, we use a novel method in which one convict cichlid fish (Amatitlania nigrofasciata) of a competing pair was startled independently of the opponent. Fish were given various opponents and the mean startle duration determined. This mean was negatively correlated with the mean use of highly escalated ‘frontal activities’ such as biting and frontal display, but not the less escalated lateral displays or tail beating. Thus the startle duration was a reliable surrogate measure of the most escalated components of aggressive interactions. That is, it provided a motivational probe for aggressiveness of individual fish. Fight motivation is often determined in terms of fight duration or physiological costs for losers, who reveal the costs they are prepared to pay. We discuss various potential advantages of the motivational probe over previous measures, particularly with respect to winners and losers and different times during the interactions.     

Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish

Variation in gene expression contributes to ecological speciation by facilitating population persistence in novel environments. Likewise, immune responses can be of relevance in speciation driven by adaptation to different environments. Previous studies examining gene expression differences between recently diverged ecotypes have often relied on only one pair of populations, targeted the expression of only a subset of genes or used wild‐caught individuals. Here, we investigated the contribution of habitat‐specific parasites and symbionts and the underlying immunological abilities of ecotype hosts to adaptive divergence in lake–river population pairs of the cichlid fish Astatotilapia burtoni. To shed light on the role of phenotypic plasticity in adaptive divergence, we compared parasite and microbiota communities, immune response, and gene expression patterns of fish from natural habitats and a lake‐like pond set‐up. In all investigated population pairs, lake fish were more heavily parasitized than river fish, in terms of both parasite taxon composition and infection abundance. The innate immune response in the wild was higher in lake than in river populations and was elevated in a river population exposed to lake parasites in the pond set‐up. Environmental differences between lake and river habitat and their distinct parasite communities have shaped differential gene expression, involving genes functioning in osmoregulation and immune response. Most changes in gene expression between lake and river samples in the wild and in the pond set‐up were based on a plastic response. Finally, gene expression and bacterial communities of wild‐caught individuals and individuals acclimatized to lake‐like pond conditions showed shifts underlying adaptive phenotypic plasticity.     

Environment-dependent inbreeding depression: its ecological and evolutionary significance

Inbreeding depression is a major evolutionary and ecological force that influences population dynamics and the evolution of inbreeding-avoidance traits such as mating systems and dispersal. There is now compelling evidence that inbreeding depression is environment-dependent. Here, we discuss ecological and evolutionary consequences of environment-dependent inbreeding depression. The environmental dependence of inbreeding depression may be caused by environment-dependent phenotypic expression, environment-dependent dominance, and environment-dependent natural selection. The existence of environment-dependent inbreeding depression challenges classical models of inbreeding as caused by unconditionally deleterious alleles, and suggests that balancing selection may shape inbreeding depression in natural populations; loci associated with inbreeding depression in some environments may even contribute to adaptation to others. Environment-dependent inbreeding depression also has important, often neglected, ecological and evolutionary consequences: it can influence the demography of marginal or colonizing populations and alter adaptive optima of mating systems, dispersal, and their associated traits. Incorporating the environmental dependence of inbreeding depression into theoretical models and empirical studies is necessary for understanding the genetic and ecological basis of inbreeding depression and its consequences in natural populations.     

Niche divergence facilitated by fine‐scale ecological partitioning in a recent cichlid fish adaptive radiation

Ecomorphological differentiation is a key feature of adaptive radiations, with a general trend for specialization and niche expansion following divergence. Ecological opportunity afforded by invasion of a new habitat is thought to act as an ecological release, facilitating divergence, and speciation. Here, we investigate trophic adaptive morphology and ecology of an endemic clade of oreochromine cichlid fishes (Alcolapia) that radiated along a herbivorous trophic axis following colonization of an isolated lacustrine environment, and demonstrate phenotype‐environment correlation. Ecological and morphological divergence of the Alcolapia species flock are examined in a phylogenomic context, to infer ecological niche occupation within the radiation. Species divergence is observed in both ecology and morphology, supporting the importance of ecological speciation within the radiation. Comparison with an outgroup taxon reveals large‐scale ecomorphological divergence but shallow genomic differentiation within the Alcolapia adaptive radiation. Ancestral morphological reconstruction suggests lake colonization by a generalist oreochromine phenotype that diverged in Lake Natron to varied herbivorous morphologies akin to specialist herbivores in Lakes Tanganyika and Malawi.     

Population genomic tests of models of adaptive radiation in Lake Victoria region cichlid fish

Adaptive radiation is usually thought to be associated with speciation, but the evolution of intraspecific polymorphisms without speciation is also possible. The radiation of cichlid fish in Lake Victoria (LV) is perhaps the most impressive example of a recent rapid adaptive radiation, with 600+ very young species. Key questions about its origin remain poorly characterized, such as the importance of speciation versus polymorphism, whether species persist on evolutionary time scales, and if speciation happens more commonly in small isolated or in large connected populations. We used 320 individuals from 105 putative species from Lakes Victoria, Edward, Kivu, Albert, Nabugabo and Saka, in a radiation-wide amplified fragment length polymorphism (AFLP) genome scan to address some of these questions. We demonstrate pervasive signatures of speciation supporting the classical model of adaptive radiation associated with speciation. A positive relationship between the age of lakes and the average genomic differentiation of their species, and a significant fraction of molecular variance explained by above-species level taxonomy suggest the persistence of species on evolutionary time scales, with radiation through sequential speciation rather than a single starburst. Finally the large gene diversity retained from colonization to individual species in every radiation suggests large effective population sizes and makes speciation in small geographical isolates unlikely.     

Depth equilibration of a shallow-water cichlid fish

The cichlid Melanochromis exasperatus has a natural distribution which is restricted to a single island in Lake Malawi, Africa. Diving observations indicated that it does not occur below 4.5 m depth. Measurements of depth equilibration in a pressure tank showed that males can equilibrate to a depth of 25 m and females to 18 m. Mean maximum sustained rate of depth equilibration was 2 m day⁻¹. M. exasperatus survived a pressure decrease of 40% every 12 h from the maximum equilibration depth to the surface. The fish swim actively during the day but rest on the bottom at night when they are equilibrated to a depth 1 m deeper than ambient. Reduced activity at night is reflected in a drop in oxygen consumption to nearly half of the daytime active value.     

Color change and pigmentation in a color polymorphic cichlid fish

Hydrobiologia - In many haplochromine cichlids, body coloration is an important communication cue during social interactions. In some cichlids, individuals can change color, but we have little...     

Mate size and breeding success in a monogamous cichlid fish

Synopsis The patterns of mate size and parental care of a monogamous cichlid fish,Cichlasoma maculicauda, were studied in Gatun Lake, Panama. Males defend territories which serve as courtship and nest sites. Within a population most mates in pairs are of equal size rank. In each pair the male is larger than the female, probably because most mature males are larger than most mature females. Clutch size increases with female body size. Male size affects breeding success in two ways. First, larger males provide nest sites less susceptible to destructive wave action. Second, young of larger males grow faster than young of smaller males. Large males defeat small males in contests for position in feeding areas, and this may provide their young with better feeding conditions. In the laboratory young growth rates increase with food abundance, and at high levels of food surpass those observed in nature. Fast growth of young reduces their vulnerability to predators and should allow parents to breed more often. Young survival rates improve with the size of the parents, so that larger fish raise more offspring at each breeding attempt. These observations suggest why preference for large mates should occur.     

Parental response to brood size in a cichlid fish

This paper reports on an experiment designed to investigate whether guarding females of the cichlid Aequidens coeruleopunctatus adjust their parental behaviour in response to changes in brood size. It was found that females were easier to scare away from their broods when threatened, and stayed away for longer, after some of their fry had been removed, and that the reverse occurred when broods were experimentally augmented with foreign fry. Brood size manipulations change the expected benefits of future investment. These results therefore indicate that parental care strategies in A. coeruleopunctatus reflect future prospects for reproductive success rather than past investment.     

A test of time-place learning in a cichlid fish

This paper presents a test of time-place learning in fish. Convict cichlids, Cichlasoma nigrofasciatum, were offered food several times a day for 10–30 consecutive days. A signal was given 1 min before each food presentation. If the food was always delivered in the same corner of the aquarium, the fish spent 66% of their time in that corner after the signal was given. But if the food was given in different corners throughout the day, each corner being associated with a specific daily time, the fish failed to show preference for the target corner, even after 30 days. Instead they learned which corners yielded food at any time of the day and visited these corners successively after the feeding signal was given. Failure to associate time and place may have been caused by a low cost of travel between corners, a limited number of rewards each day, and / or interference from learning the signal-food association.