Adaptive responses in resurgent Lake Victoria cichlids over the past 30 years

Textbook examples of adaptive radiation often show rapid morphological changes in response to environmental perturbations. East Africa's Lake Victoria, famous for its stunning adaptive radiation of cichlids, has suffered from human-induced eutrophication over the past decades. This cultural eutrophication is thought to be partly responsible for the dramatically reduced cichlid biodiversity, but climatic variability in itself might also have contributed to the eutrophication which resulted in low oxygen levels and decreased water transparency. To determine how recent environmental changes have influenced the lake and its cichlids over the past 50years, we gathered environmental and meteorological variables and compared these with gill surface area of four cichlid species. We found that during the period of severe eutrophication and temperature increase (1980s), reduced wind speeds coincided with a reduction in oxygen levels and a decrease in both water temperature and transparency. The gill surface area in three out of the four cichlid species increased during this period which is consistent with adaptive change in response to increased hypoxia. During the 2000s, wind speeds, oxygen levels, water transparency and water temperature increased again, while cichlid gill surface area decreased. Our results imply that climatic changes and especially wind speed and direction might play a crucial role in tropical lake dynamics. The changes in Lake Victoria's water quality coincide with fluctuations in cichlid gill surface area, suggesting that these fish can respond rapidly to environmental perturbations, but also that climatic variability, together with continued eutrophication, might be detrimental to the lake's cichlid biodiversity.

Rapid morphological changes in response to fluctuating natural environments are a common phenomenon in species that undergo adaptive radiation. The dramatic ecological changes in Lake Victoria provide a unique opportunity to study environmental effects on cichlid morphology. This study shows how four haplochromine cichlids adapted their premaxilla to a changed diet over the past 30 years. Directly after the diet change toward larger and faster prey in the late 1980s, the premaxilla (upper jaw) changed in a way that is in agreement with a more food manipulating feeding style. During the 2000s, two zooplanktivorous species showed a reversal of morphological changes after returning to their original diet, whereas two other species showed no reversal of diet and morphology. These rapid changes indicate a potential for extremely fast adaptive responses to environmental fluctuations, which are likely inflicted by competition release and increase, and might have a bearing on the ability of haplochromines to cope with environmental changes. These responses could be due to rapid genetic change or phenotypic plasticity, for which there is ample evidence in cichlid fish structures associated with food capture and processing. These versatile adaptive responses are likely to have contributed to the fast adaptive radiation of haplochromines.

The kidney histology of silver sea bream Sparus sarba adapted to different salinities was studied. Renal glomeruli in silver sea bream were grouped into clusters and two distinct types of glomeruli could be discerned. Expanded glomeruli were highly vascular, probably related to an active filtering role, while collapsed glomeruli had a shrunken appearance, probably related to an abated filtering role. Collecting tubules were lined by tall columnar cells and were more prominent and muscular in hypo‐osmotic media. Chronic adaptation across a broad spectrum of salinities (0, 6, 12, 33 and 50) caused significant modifications in renal morphology. In hypo‐osmotic media, a significant increase in glomerular number, size and percentage expanded glomeruli were found, which could facilitate water excretion. Collecting tubules exhibited an increase in thickness, diameter and muscularity that tended to favour a faster glomerular filtrate flow upon hypo‐osmotic adaptation. Abrupt hypo‐osmotic exposure induced rapid changes in the morphology of renal tubules. There was an increase in diameter and thickness of collecting tubules, suggesting increased glomerular filtrate flow was stimulated by hypo‐osmotic exposure. The data suggested that the rapid change in kidney morphology is one of the osmoregulatory strategies of silver sea bream that may contribute to its ability to withstand abrupt hypo‐osmotic challenge. A fast‐acting mechanism that could be triggered within several hours could reorganize silver sea bream kidney so that the renal machinery is highly responsive to changes in environmental salinities.

Acclimatization through phenotypic plasticity represents a more rapid response to environmental change than adaptation and is vital to optimize organisms' performance in different conditions. Generally, animals are less phenotypically plastic than plants, but reef-building corals exhibit plant-like properties. They are light dependent with a sessile and modular construction that facilitates rapid morphological changes within their lifetime. We induced phenotypic changes by altering light exposure in a reciprocal transplant experiment and found that coral plasticity is a colony trait emerging from comprehensive morphological and physiological changes within the colony. Plasticity in skeletal features optimized coral light harvesting and utilization and paralleled significant methylome and transcriptome modifications. Network-associated responses resulted in the identification of hub genes and clusters associated to the change in phenotype: inter-partner recognition and phagocytosis, soft tissue growth and biomineralization. Furthermore, we identified hub genes putatively involved in animal photoreception-phototransduction. These findings fundamentally advance our understanding of how reef-building corals repattern the methylome and adjust a phenotype, revealing an important role of light sensing by the coral animal to optimize photosynthetic performance of the symbionts.

CD45 is a transmembrane protein tyrosine phosphatase required for signal transduction through the Ag receptor complexes of T and B lymphocytes. Herein, we demonstrate that immobilized mAbs to the external domain of CD45 induce rapid and dramatic morphologic changes in a variety of T cell lines, including CD8+ cytotoxic clones. CD45-induced morphologic changes can be inhibited by the cytoskeletal inhibitors cytochalasin D and E and by the protein tyrosine kinase inhibitor herbimycin A. Consistent with the requirement for tyrosine kinase activity, tyrosine phosphorylation of proteins at about 60 to 75 kDa and 115 to 130 kDa is increased upon engagement with immobilized anti-CD45 mAb with kinetics paralleling the observed changes in morphology. The phosphorylation of these proteins is inhibited by tyrosine kinase inhibitors at concentrations that also inhibit changes in morphology. The phosphoproteins induced when cells are added to immobilized anti-CD45 are co-immunoprecipitated with p56lck, suggesting that this tyrosine kinase might play a role in the phosphorylation of these proteins. Consistent with this, there is no increase in the phosphorylation of these proteins in p56lck-deficient CTLL-2 cells in response to immobilized anti-CD45 mAb. An important role for p56lck in the morphologic pathway is further supported by the observation that p56lck-deficient human J.CAM1.6 cells, in contrast to the parental Jurkat line, cannot be induced to undergo morphologic changes. Taken together, these results suggest a possible role for CD45 in coordinating a cytoskeletal remodeling cascade that may be important in cell activation.

The transformation of Lake Victoria that began in 1980 followed the population explosion of Nile perch Lates niloticus, causing the apparent extirpation of 500+ endemic haplochromine species and dramatic physico-chemical changes. Officially introduced in 1962–1963, but present earlier, the reasons for the long delay before its population exploded are discussed. The hypothesis that it occurred only after the haplochromine decline is evaluated, but haplochromines declined only after the Nile perch expansion began. The sudden eutrophication of the lake was attributed to Nile perch, but evidence of eutrophication from 1950 onwards led some researchers to conclude that it was the result of climatic changes. We conclude that the haplochromine destruction disrupted the complex food webs that existed prior to the upsurge of Nile perch. The depletion of fish biomass by Nile perch may have been the source of extra phosphorus responsible for the eutrophication of the lake. After the Nile perch explosion in 1980 the fish population came to be dominated by only three species, but fisheries productivity increased at least 10-fold. Fishing has caused demographic changes in Nile perch, which may have allowed some haplochromine species to recover. The condition of the lake appears to have stabilised since 2000, partly because the fish biomass has risen to at least 2 × 106 t, replacing the ‘lost’ biomass and restoring some ecosystem functioning.

Understanding the “origin of species” has been one of the major topics in biology ever since Charles Darwin’s famous publication (Darwin 1859). One and a half centuries later speciation still remains the “mystery of mysteries” (Pennisi 2005). While we have learned a lot from traditional laboratory model organisms, we now realize that many questions in speciation research can only be answered by studying how organisms adapt, behave and diversify in their natural environment (Nosil et al. 2017). Some of the main questions in speciation research at the moment are: “Which barriers contribute to reproductive isolation?”, “What are the genomic patterns of reproductive isolation?”, “What is the role of plasticity? ”, and “What is the role of changes in gene expression” (Butlin et al. 2012). With this thesis I aim to provide part of the answers to these questions by studying one of the best model systems for speciation research: the East African cichlid fishes (Kocher 2004). Astatotilapia burtoni is a haplochromine cichlid that inhabits both Lake Tanganyika and affluent rivers. Lake and river populations of A. burtoni represent an emerging model system for studying early phases of adaptive divergence. In my thesis, I investigate the degree of reproductive isolation between different populations and the mechanisms that drive the lake-stream divergence. More specifically, I characterize the reproductive barriers contributing to reproductive isolation and investigate the roles of local adaptation, adaptive phenotypic plasticity, parasites, immune system response, and gene expression in lake-stream divergence. The main body of work includes four chapters on East-African haplochromine cichlid fishes as a model for studying early phases of adaptive divergence. In Chapter 1, I investigate the relative contributions of adaptive phenotypic plasticity versus local adaptation to fitness of A. burtoni populations from Lake Tanganyika and nearby rivers. Adaptive phenotypic plasticity has previously been proposed to play a key role in the impressive radiations of cichlids. However, mostly due to logistic difficulties, field-experiments are scarce in this system. By performing two transplant experiments in Lake Tanganyika, using both wild caught and common garden raised F1 individuals, I provide one of the first field-based experiments to assess direct fitness consequences of morphological and genetic divergence between lake and stream cichlids in nature. In Chapter 2, I further investigate the correlation between genetic divergence between populations and the level of reproductive isolation between populations by performing a mesocosm mating experiment in a semi-natural setting at Lake Tanganyika. I assessed reproductive isolation in the presence of male-male competition by analysing survival and growth rates of introduced adults and their reproductive success from genetic parentage of surviving offspring. I provide one of the first field-based experiments to assess multiple environment dependent (extrinsic) components of reproductive isolation in cichlids. In Chapter 3, I investigate the role of ecotype-specific parasites, the immune response of hosts, and gene expression in the lake-stream divergence. By performing parasitological screening, immune response measurements, and RNA-sequencing of immune-related organs of fish from natural habitats as well as a lake-like pond setup I reveal the mechanisms underlying phenotypic plasticity in this system. In Chapter 4, three other haplochromine cichlid species that co-exist with A. burtoni in Lake Tanganyika and surrounding drainage systems were used to uncover commonalities and differences in adaptation to the river/lake habitat. We sequenced whole genomes of multiple lake- stream population pairs of A. burtoni and Ctenochromis horei, Haplochromis stappersi, and Pseudocrenilabrus philander. These natural replicates offered a unique possibility to test whether the same patterns and processes are involved in the adaptation to the lake-stream transition in four haplochromine species. I performed landmark-based geometric morphometric analysis on digital images of fishes of the four species to capture disparity in body shape and compare it with genomic disparity.

Pressure Overload Induces Early Morphological Changes in the Heart

Cichlids are an excellent model to study explosive speciation and adaptive radiation. Their evolutionary success has been attributed to their ability to undergo rapid morphological changes related to diet, and their particular breeding biology. Relatively minor changes in morphology allow for exploitation of novel food resources. The importance of phenotypic plasticity and genetically based differences for diversification was long recognized, but their relationship and relative magnitude remained unclear. We compared morphology of individuals of four wild populations of the Lake Tanganyika cichlid Tropheus moorii with their pond-raised F1 offspring. The magnitude of morphological change via phenotypic plasticity between wild and pond-bred F1 fish exceeds pairwise population differences by a factor of 2.4 (mean Mahalanobis distances). The genetic and environmental effects responsible for among population differentiation in the wild could still be recognized in the pond-bred F1 fish. All four pond populations showed the same trends in morphological change, mainly in mouth orientation, size and orientation of fins, and thickness of the caudal peduncle. As between population differentiation was lower in the wild than differentiation between pond-raised versus wild fish, we suggest the narrow ecological niche and intense interspecific competition in rock habitats is responsible for consistent shape similarity, even among long-term isolated populations.Electronic supplementary materialThe online version of this article (doi:10.1007/s00114-010-0751-2) contains supplementary material, which is available to authorized users.

Whitefish, genus Coregonus, show exceptional levels of phenotypic diversity with sympatric morphs occurring in numerous postglacial lakes in the northern hemisphere. Here, we studied the effects of human-induced eutrophication on sympatric whitefish morphs in the Swiss lake, Lake Thun. In particular, we addressed the questions whether eutrophication (i) induced hybridization between two ecologically divergent summer-spawning morphs through a loss of environmental heterogeneity, and (ii) induced rapid adaptive morphological changes through changes in the food web structure. Genetic analysis based on 11 microsatellite loci of 282 spawners revealed that the pelagic and the benthic morph represent highly distinct gene pools occurring at different relative proportions on all seven known spawning sites. Gill raker counts, a highly heritable trait, showed nearly discrete distributions for the two morphs. Multilocus genotypes characteristic of the pelagic morph had more gill rakers than genotypes characteristic of benthic morph. Using Bayesian methods, we found indications of recent but limited introgressive hybridization. Comparisons with historical gill raker data yielded median evolutionary rates of 0.24 haldanes and median selection intensities of 0.27 for this trait in both morphs for 1948-2004 suggesting rapid evolution through directional selection at this trait. However, phenotypic plasticity as an alternative explanation for this phenotypic change cannot be discarded. We hypothesize that both the temporal shifts in mean gill raker counts and the recent hybridization reflect responses to changes in the trophic state of the lake induced by pollution in the 1960s, which created novel selection pressures with respect to feeding niches and spawning site preferences.

Abrogation of microcystin cytotoxicity by MAP kinase inhibitors and N-acetyl cysteine is confounded by OATPIB1 uptake activity inhibition

As in Lake Victoria and Lake Kyoga, most of the native fish species of Lake Nabugabo have either been depleted or have disappeared since Lates niloticus, Nile perch, and Oreochromis niloticus, a tilapiine, were introduced. L. niloticus, O. niloticus, Schilbe intermedius, Brycinus jacksonii, and Rastrineobola argentea are the only species still abundant and widespread in the lake. Of the five haplochromine species endemic to Lake Nabugabo, at least one has vanished and the remaining ones are very rare. The prey of the Nile perch in Lake Nabugabo, with the exception of the prawn Caridina nilotica, which is absent from the lake, are similar to those the predator switched to in Lakes Victoria and Kyoga after haplochromines had been depleted. These consist of ephemeropterans—especially Povilla, the anisopteran nymphs R. argentea, tilapiines, and juvenile Nile perch. Three small lakes adjacent to Lake Nabugabo—Lake Kayanja, Lake Kayugi, and Lake Manywa—contain large numbers of Oreochromis esculentus and two haplochromine species previously known only in Lake Nabugabo. These three lakes should be designated conservation areas for the cichlids and other native species that were previously abundant in Lakes Victoria, Kyoga, and Nabugabo. The swamps around these lakes should be protected so that the Nile perch does not spread into them. Further research should be carried out to ensure the preservation of the endemic species.

The pancake tortoise Malacochersus tornieri (Siebenrock 1903) of East Africa is morphologically, behaviourally and ecologically unique among extant land tortoises of the family Testudinidae. Recent studies suggest it shares a common ancestor with the Indotestudo – Testudo group, but the selective pressures and evolutionary pathway that produced the single extant species, Malacochersus tornieri, are poorly understood. We propose that intense predation pressure and competition initiated the process of change from an ancestral, generalized tortoise form by driving Malacochersus into rocky areas and subsequently rock crevices, where predation and competition were reduced. This change in habitat led to rapid changes in morphology, ecology, and behaviour in order to better adapt to the crevice environment, and to enhance its safety within from predators. These changes in turn led to strict limits to the extent and duration of out-of-crevice activity. The changes in morphology also allowed greater mobility, agility, and speed to enhance safety when tortoises left their crevices to forage, mate, defecate, or colonize new habitats. Padlopers, an extant clade of small, southern African tortoises may provide insight into the pancake tortoise’s ancestral evolution toward its modern form, lifestyle, and reproductive characteristics. Both the pancake tortoise and padlopers also inexplicably display an unusually large amount of anomalous variation in scute and/or shell characteristics.

Protein kinase C and phorbol ester receptor expression related to growth and differentiation of nullipotent and pluripotent embryonal carcinoma cells

Adaptive Phenotypic Plasticity: Target or By-Product of Selection in a Variable Environment?