What is ecological speciation

Carotenoids contribute significantly to animal body coloration, including the spectacular color pattern diversity among fishes. Fish, as other animals, derive carotenoids from their diet. Following uptake, transport and metabolic conversion, carotenoids allocated to body coloration are deposited in the chromatophore cells of the integument. The genes involved in these processes are largely unknown. Using RNA-Sequencing, we tested for differential gene expression between carotenoid-colored and white skin regions of a cichlid fish, Tropheus duboisi “Maswa”, to identify genes associated with carotenoid-based integumentary coloration. To control for positional gene expression differences that were independent of the presence/absence of carotenoid coloration, we conducted the same analyses in a closely related population, in which both body regions are white. A larger number of genes (n = 50) showed higher expression in the yellow compared to the white skin tissue than vice versa (n = 9). Of particular interest was the elevated expression level of bco2a in the white skin samples, as the enzyme encoded by this gene catalyzes the cleavage of carotenoids into colorless derivatives. The set of genes with higher expression levels in the yellow region included genes involved in xanthophore formation (e.g., pax7 and sox10), intracellular pigment mobilization (e.g., tubb, vim, kif5b), as well as uptake (e.g., scarb1) and storage (e.g., plin6) of carotenoids, and metabolic conversion of lipids and retinoids (e.g., dgat2, pnpla2, akr1b1, dhrs). Triglyceride concentrations were similar in the yellow and white skin regions. Extracts of integumentary carotenoids contained zeaxanthin, lutein and beta-cryptoxanthin as well as unidentified carotenoid structures. Our results suggest a role of carotenoid cleavage by Bco2 in fish integumentary coloration, analogous to previous findings in birds. The elevated expression of genes in carotenoid-rich skin regions with functions in retinol and lipid metabolism supports hypotheses concerning analogies and shared mechanisms between these metabolic pathways. Overlaps in the sets of differentially expressed genes (including dgat2, bscl2, faxdc2 and retsatl) between the present study and previous, comparable studies in other fish species provide useful hints to potential carotenoid color candidate genes.

/pdf/comparative-transcriptomics-reveals-candidate-carotenoid-4ncx4htmzp.pdf

Comparative transcriptomics reveals candidate carotenoid color genes in an East African cichlid fish

Sexual imprinting—a phenomenon in which offspring learn parental traits and later use them as a model for their own mate preferences—can generate reproductive barriers between species1. When the target of imprinting is a mating trait that differs among young lineages, imprinted preferences may contribute to behavioural isolation and facilitate speciation1,2. However, in most models of speciation by sexual selection, divergent natural selection is also required; the latter acts to generate and maintain variation in the sexually selected trait or traits, and in the mating preferences that act upon them3. Here we demonstrate that imprinting, in addition to mediating female mate preferences, can shape biases in male–male aggression. These biases can act similarly to natural selection to maintain variation in traits and mate preferences, which facilitates reproductive isolation driven entirely by sexual selection. Using a cross-fostering study, we show that both male and female strawberry poison frogs (Oophaga pumilio) imprint on coloration, which is a mating trait that has diverged recently and rapidly in this species4. Cross-fostered females prefer to court mates of the same colour as their foster mother, and cross-fostered males are more aggressive towards rivals that share the colour of their foster mother. We also use a simple population-genetics model to demonstrate that when both male aggression biases and female mate preferences are formed through parental imprinting, sexual selection alone can (1) stabilize a sympatric polymorphism and (2) strengthen the trait–preference association that leads to behavioural reproductive isolation. Our study provides evidence of imprinting in an amphibian and suggests that this rarely considered combination of rival and sexual imprinting can reduce gene flow between individuals that bear divergent mating traits, which sets the stage for speciation by sexual selection. Tadpoles of strawberry poison frogs (Oophaga pumilio) are shown to imprint on adult coloration, affecting both male aggression biases and female preferences and setting the stage for speciation by sexual selection.

Imprinting sets the stage for speciation

Many reptiles and some fish determine offspring sex by environmental cues such as incubation temperature. The mechanism by which environmental signals are captured and transduced into specific sexual phenotypes has remained unexplained for over 50 years. Indeed, environmental sex determination (ESD) has been viewed as an intractable problem because sex determination is influenced by a myriad of genes that may be subject to environmental influence. Recent demonstrations of ancient, conserved epigenetic processes in the regulatory response to environmental cues suggest that the mechanisms of ESD have a previously unsuspected level of commonality, but the proximal sensor of temperature that ultimately gives rise to one sexual phenotype or the other remains unidentified. Here, we propose that in ESD species, environmental cues are sensed by the cell through highly conserved ancestral elements of calcium and redox (CaRe) status, then transduced to activate ubiquitous signal transduction pathways, or influence epigenetic processes, ultimately to drive the differential expression of sex genes. The early evolutionary origins of CaRe regulation, and its essential role in eukaryotic cell function, gives CaRe a propensity to be independently recruited for diverse roles as a 'cellular sensor' of environmental conditions. Our synthesis provides the first cohesive mechanistic model connecting environmental signals and sex determination pathways in vertebrates, providing direction and a framework for developing targeted experimentation.

Cellular calcium and redox regulation: the mediator of vertebrate environmental sex determination?

The evolution of territoriality reflects the balance between the benefit and cost of monopolising a resource. While the benefit of territoriality is generally intuitive (improved access to resources), our understanding of its cost is less clear. This paper combines: 1. a review of hypotheses and meta-analytic benchmarking of costs across diverse taxa; and 2. a new empirical test of hypotheses using a longitudinal study of free-living male territorial lizards. The cost of territoriality was best described as a culmination of multiple factors, but especially costs resulting from the time required to maintain a territory (identified by the meta-analysis) or those exacerbated by a territory that is large in size (identified by the empirical test). The meta-analysis showed that physiological costs such as energetic expenditure or stress were largely negligible in impact on territory holders. Species that used territories to monopolise access to mates appeared to incur the greatest costs, whereas those defending food resources experienced the least. The single largest gap in our current understanding revealed by the literature review is the potential cost associated with increased predation. There is also a clear need for multiple costs to be evaluated concurrently in a single species. The empirical component of this study showcases a powerful analytical framework for evaluating a range of hypotheses using correlational data obtained in the field. More broadly, this paper highlights key factors that should be considered in any investigation that attempts to account for the evolutionary origin or ecological variation in territorial behaviour within and between species.

https://link.springer.com/content/pdf/10.1007/s00442-021-05068-6.pdf

Costs of territoriality: a review of hypotheses, meta-analysis, and field study

Dominance hierarchies are a fundamental part of social systems in many species and social rank can influence access to resources and impact health and physiology. While social subordination is a profound stressor, few studies consider the social stress experienced by dominant males due to constantly needing to defend their dominance status through costly aggressive displays. Recent studies suggest that in species that use body coloration to signal status, these costs may also be color morph-specific. Our study examines the link between the social rank, intensity of territorial defense, body coloration, and oxidative stress in males of the color polymorphic cichlid fish Astatotilapia burtoni where males are either blue or yellow. We studied behavior in naturalistic communities and examined circulating reactive oxygen metabolites (ROMs) and antioxidant defenses. We found that dominant males experience higher concentrations of circulating ROMs without notably increasing their antioxidant defenses, but this effect was not related to color morph. Aggression and social network ties predicted oxidative stress in a morph-specific manner, with yellow but not blue males showing signs of increased oxidative damage with increasing agonistic effort. In contrast to expectation, oxidative stress was not influenced by cortisol or testosterone levels. We conclude that oxidative stress is instrumental to understanding the costs and benefits of high social rank. Living in a social hierarchy can be stressful even for those on top. While past work has established the stress involved in being a low-ranking member of a hierarchy, we show that while high-ranking males attain definite advantages in terms of decreased stress hormone levels and increased reproductive opportunities, they also pay for their increased activity level with increased risk of cellular damage.

Social rank, color morph, and social network metrics predict oxidative stress in a cichlid fish

Social network stability is impacted by removing a dominant male in replicate dominance hierarchies of a cichlid fish

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 information about the underlying physiological mechanisms. We examined the regulation of coloration in the color polymorphic cichlid fish Astatotilapia burtoni where males are either blue or yellow. Previous studies implicated the melanocortin system, a neuroendocrine center that regulates pigmentation and the stress response, in regulating the color polymorphism in this species. We found that both blue and yellow males express a high density of yellow xanthophores. Dispersal of xanthophore pigments in both yellow and blue morphs occurred within minutes in a dose-dependent manner. Similarly, exogenous α-melanocyte stimulating hormone (α-MSH, a melanocortin hormone) increased yellowness of the body in a dose-independent fashion. We observed many color changes in males housed in social communities with the proportion of yellow males increasing over the 2-week experimental period. However, color phenotype or color change was not influenced by experimental alteration of the stability of the social hierarchy. The effects of α-MSH suggest that the melanocortin system contributes to the polymorphism in coloration in A. burtoni but the role of social interactions and social stress in regulating color remains unclear.

Color change and pigmentation in a color polymorphic cichlid fish

Experimental reduction of a nest ectoparasite affects mouth coloration of nestling Cliff Swallows Petrochelidon pyrrhonota

Oxidative stress is a potential cost of social dominance and reproduction, which could mediate life history trade-offs between current and future reproductive fitness. However, the evidence for an oxidative cost of social dominance and reproduction is mixed, in part because organisms have efficient protective mechanisms that can counteract oxidative insults. Further, previous studies have shown that different aspects of oxidative balance, including oxidative damage and antioxidant function, vary dramatically between tissue types, yet few studies have investigated oxidative cost in terms of interconnectedness and coordination within the system. Here, we tested whether dominant and subordinate males of the cichlid Astatotilapia burtoni differ in integration of different components of oxidative stress. We assessed 7 markers of oxidative stress, which included both oxidative damage and antioxidant function in various tissue types (total of 14 measurements). Across all oxidative stress measurements, we found more co-regulated clusters in dominant males, suggesting that components of oxidative state are more functionally integrated in dominant males than they are in subordinate males. We discuss how a high degree of functional integration reflects increased robustness or efficiency of the system (e.g. increased effectiveness of antioxidant machinery in reducing oxidative damage), but we also highlight potential costs (e.g. activation of cytoprotective mechanisms may have unwanted pleiotropic effects). Overall, our results suggest that quantifying the extent of functional integration across different components of oxidative stress could reveal insights into the oxidative cost of important life history events. 

Social dominance and reproduction result in increased integration of oxidative state in males of an African cichlid fish.

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