The shared-pathway hypothesis offers a cellular explanation for the connection between ketocarotenoid pigmentation and individual quality. Under this hypothesis, ketocarotenoid metabolism shares cellular pathways with mitochondrial oxidative phosphorylation such that red carotenoid-based coloration is inextricably linked mitochondrial function. To test this hypothesis, we exposed Tigriopus californicus copepods to a mitochondrially targeted protonophore, 2,4-dinitrophenol (DNP), to induce proton leak in the inner mitochondrial membranes. We then measured whole-animal metabolic rate and ketocarotenoid accumulation. As observed in prior studies of vertebrates, we observed that DNP treatment of copepods significantly increased respiration and that DNP-treated copepods accumulated more ketocarotenoid than control animals. Moreover, we observed a relationship between ketocarotenoid concentration and metabolic rate, and this association was strongest in DNP-treated copepods. These data support the hypothesis that ketocarotenoid and mitochondrial metabolism are biochemically intertwined. Moreover, these results corroborate observations in vertebrates, perhaps suggesting a fundamental connection between ketocarotenoid pigmentation and mitochondrial function that should be explored further.
- Award ID(s):
- NSF-PAR ID:
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Page Range / eLocation ID:
- 1811 to 1826
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
Even as numerous studies have documented that the red and yellow coloration resulting from the deposition of carotenoids serves as an honest signal of condition, the evolution of condition dependency is contentious. The resource trade‐off hypothesis proposes that condition‐dependent honest signalling relies on a trade‐off of resources between ornamental display and body maintenance. By this model, condition dependency can evolve through selection for a re‐allocation of resources to promote ornament expression. By contrast, the index hypothesis proposes that selection focuses mate choice on carotenoid coloration that is inherently condition dependent because production of such coloration is inexorably tied to vital cellular processes. These hypotheses for the origins of condition dependency make strongly contrasting and testable predictions about ornamental traits. To assess these two models, we review the mechanisms of production of carotenoids, patterns of condition dependency involving different classes of carotenoids, and patterns of behavioural responses to carotenoid coloration. We review evidence that traits can be condition dependent without the influence of sexual selection and that novel traits can show condition‐dependent expression as soon as they appear in a population, without the possibility of sexual selection. We conclude by highlighting new opportunities for studying condition‐dependent signalling made possible by genetic manipulation and expression of ornamental traits in synthetic biological systems.
Dam, Hans G. (Ed.)The marine copepod, Tigriopus californicus , produces the red carotenoid pigment astaxanthin from yellow dietary precursors. This ‘bioconversion’ of yellow carotenoids to red is hypothesized to be linked to individual condition, possibly through shared metabolic pathways with mitochondrial oxidative phosphorylation. Experimental inter-population crosses of lab-reared T . californicus typically produces low-fitness hybrids is due in large part to the disruption of coadapted sets nuclear and mitochondrial genes within the parental populations. These hybrid incompatibilities can increase variability in life history traits and energy production among hybrid lines. Here, we tested if production of astaxanthin was compromised in hybrid copepods and if it was linked to mitochondrial metabolism and offspring development. We observed no clear mitonuclear dysfunction in hybrids fed a limited, carotenoid-deficient diet of nutritional yeast. However, when yellow carotenoids were restored to their diet, hybrid lines produced less astaxanthin than parental lines. We observed that lines fed a yeast diet produced less ATP and had slower offspring development compared to lines fed a more complete diet of algae, suggesting the yeast-only diet may have obscured effects of mitonuclear dysfunction. Astaxanthin production was not significantly associated with development among lines fed a yeast diet but was negatively related to development in early generation hybrids fed an algal diet. In lines fed yeast, astaxanthin was negatively related to ATP synthesis, but in lines fed algae, the relationship was reversed. Although the effects of the yeast diet may have obscured evidence of hybrid dysfunction, these results suggest that astaxanthin bioconversion may still be related to mitochondrial performance and reproductive success.more » « less
Human activities are altering natural ecosystems, leading to widespread environmental change that can vary across spatiotemporal scales, thus creating dynamic, novel conditions at both large and small scales. In highly disturbed aquatic systems, elevated turbidity is one common stressor that alters the sensory environment of fishes and can disrupt communication, including mate choice, driving population‐level shifts in visual communication traits such as nuptial coloration. At a smaller, within‐population scale, we can expect similar adaptive divergence to a heterogeneous visual landscape. Using the cichlid fish,
Pseudocrenilabrus multicolor,we investigated within‐population variation in diet and nuptial coloration by sampling fish from microhabitats within a relatively small site (~0.14 km2). These visual microhabitats are affected by different types of human disturbance at a very small scale leading to significant differences in water clarity (i.e. turbidity). We used three, non‐mutually exclusive working hypotheses to test if (1) males in low turbidity invest more in carotenoid‐based coloration (economy of pigments hypothesis), (2) fish from low‐turbidity sites eat more carotenoid‐rich foods (diet hypothesis), and (3) fish are habitat matching. Stomach content analyses revealed relatively high overlap in diet across microhabitats; however, fish from stations with the lowest turbidity consumed relatively more plant material (high in carotenoid content) than fish captured at high‐turbidity stations. Males from clearer waters displayed significantly more carotenoid‐based, red and yellow coloration than fish found in microhabitats with higher turbidity, similar to between‐population color variation in this species. Furthermore, larger fish displayed more carotenoid coloration overall, but there was no difference in mean male size among microhabitats suggesting that fish were not sorting into microhabitats. Our results suggest that within‐population variation in nuptial coloration could be associated with microhabitat heterogeneity in the visual landscape driven by turbidity, a diet with more carotenoid‐rich prey items, or a combination of both.
A wide variety of species are distinguished by slight color variations. However, molecular analyses have repeatedly demonstrated that coloration does not always correspond to distinct evolutionary histories between closely related groups, suggesting that this trait is labile and can be misleading for species identification. In the present study, we analyze the evolutionary history of sister species of
Prionurussurgeonfishes in the Tropical Eastern Pacific (TEP), which are distinguished by the presence or absence of dark spots on their body. We examined the species limits in this system using comparative specimen‐based approaches, a mitochondrial gene (COI), more than 800 nuclear loci (Ultraconserved Elements), and abiotic niche comparisons. The results indicate there is a complete overlap of meristic counts and morphometric measurements between the two species. Further, we detected multiple individuals with intermediate spotting patterns suggesting that coloration is not diagnostic. Mitochondrial data recovered a single main haplotype shared between the species and all locations resulting in a complete lack of structure (ΦST = 0). Genomic analyses also suggest low levels of genetic differentiation ( FST = 0.013), and no alternatively fixed SNPs were detected between the two phenotypes. Furthermore, niche comparisons could not reject niche equivalency or similarity between the species. These results suggest that these two phenotypes are conspecific and widely distributed in the TEP. Here, we recognize Prionurus punctatusGill 1862 as a junior subjective synonym of P. laticlavius(Valenciennes 1846). The underlying causes of phenotypic variation in this species are unknown. However, this system gives insight into general evolutionary dynamics within the TEP.