Brown Morphs Research Articles

A new intertidal barnacle, Chthamalus ngankeeae sp. nov. (Balanomorpha: Chthamalidae) from the Malaysian Peninsula and western Borneo waters

The present study identified a new barnacle species from Malaysian waters, Chthamalus ngankeeae sp. nov., on morphological and molecular grounds. Chthamalus ngankeeae sp. nov. is an intertidal species that is abundant on high shores, above the oyster zone. Chthamalus ngankeeae sp. nov. has two morphotypes, based on shell colour. Brown morphs have brown shells with pale brown ridges and look similar to Microeuraphia withersi (Pilsbry, 1916). Chthamalus ngankeeae sp. nov. has four teeth on the mandible, while M. withersi has but three. White morphs of C. ngankeeae sp. nov. possess white shells with gray ridges. The white morph of C. ngankeeae sp. nov. is similar to C. moro Pilsbry, 1916, but a major morphological difference includes a more prominent articular ridge on the scutum of C. ngankeeae sp. nov. compared to C. moro. Molecular analyses of sequence divergence in the COI and NaK genes of C. ngankeeae sp. nov. with other chthamalids showed that it forms an individual monophyletic group and does not belong to any of the cryptic lineages of C. moro, supporting its designation as a new species.

Sex allocation is color morph-specific and associated with fledging condition in a wild bird.

Melanin-based color polymorphism is predicted to evolve and maintain through differential fitness of morphs in different environments, and several empirical studies indicate that life history strategies, physiology, and behavior vary among color morphs. Sex allocation theory predicts that parents should adjust their sex allocation based on differential costs of raising sons and daughters, and therefore, color morphs are expected to modify their brood sex ratio decisions. In color polymorphic tawny owls (Strix aluco), the pheomelanistic brown morph is associated with higher energy requirements, faster growth, and higher parental effort than the gray morph. As hypothesized, we find that brown tawny owl mothers produced more daughters in early broods and more males in late broods, whereas gray mothers did the opposite. At fledging, daughters of early broods and of brown mothers were heavier than those of late broods or gray mothers. Hence, larger and more costly daughters appeared to benefit more than males from being born to brown mothers early in the season. Brown mothers breeding later in the season produced more cheap sons, while gray mothers face fewer challenges under limited resources and favor daughters. These findings suggest that environmental conditions influence brood sex allocation strategies of genetically determined color morphs differently.

Genomic basis of melanin-associated phenotypes suggests colour-specific environmental adaptations in tawny owls.

Feathers comprise a series of evolutionary innovations but also harbour colour, a key biological trait known to co-vary with life history or complex traits. Those relationships are particularly true in melanin-based pigmentation species due to known pleiotropic effects of the melanocortin pathway - originating from melanin-associated phenotypes. Here, we explore the molecular basis of melanin colouration and expected co-variation at the molecular level in the melanin-based, colour polymorphic system of the tawny owl (Strix aluco). An extensive body of literature has revealed that grey and brown tawny owl colour morphs differ in a series of life history and behavioural traits. Thus, it is plausible to expect co-variation also at molecular level between colour morphs. To investigate this possibility, we assembled the first draft genome of the species against which we mapped ddRADseq reads from 220 grey and 150 brown morphs - representing 10 years of pedigree data from a population in Southern Finland - and explored genome-wide associations with colour phenotype. Our results revealed putative molecular signatures of cold adaptation strongly associated with the grey phenotype, namely, a non-synonymous substitution in MCHR1, plus 2 substitutions in non-coding regions of FTCD and FAM135A whose genotype combinations obtained a predictive power of up to 100% (predicting grey colour). These suggest a molecular basis of cold environment adaptations predicted to be grey-morph specific. Our results potentially reveal part of the molecular machinery of melanin-associated phenotypes and provide novel insights towards understanding the functional genomics of colour polymorphism in melanin-based pigmented species.

Ontogeny of color development in two green-brown polymorphic grasshopper species.

Many insects, including several orthopterans, undergo dramatic changes in body coloration during ontogeny. This variation is particularly intriguing in gomphocerine grasshoppers, where the green and brown morphs appear to be genetically determined (Schielzeth & Dieker, 2020, BMC Evolutionary Biology, 20, 63; Winter etal., 2021, Heredity, 127, 66). A better understanding of how these color morphs develop during ontogeny can provide valuable insights into the evolution and ecology of such a widespread color polymorphism. Here, we focus on the color development of two green-brown polymorphic species, the club-legged grasshopper Gomphocerus sibiricus and the steppe grasshopper Chorthippus dorsatus. By following the color development of individuals from hatching to adulthood, we found that color morph differences begin to develop during the second nymphal stage, are clearly defined by the third nymphal stage, and remain stable throughout the life of an individual. Interestingly, we also observed that shed skins of late nymphal stages are identifiable by color morphs based on their yellowish coloration, rather than the green that marks green body parts. Furthermore, by assessing how these colors are perceived by different visual systems, we found that certain potential predators can chromatically discriminate between morphs, while others may not. These results suggest that the putative genes controlling color morph are active during the early stages of ontogeny, and that green color is likely composed of two components, one present in the cuticle and one not. In addition, the effectiveness of camouflage appears to vary depending on the specific predator involved.

Regional variation in climate change alters the range-wide distribution of colour polymorphism in a wild bird.

According to Gloger's rule, animal colouration is expected to be darker in wetter and warmer climates. Such environmental clines are predicted to occur in colour polymorphic species and to be shaped by selection if colour morphs represent adaptations to different environments. We studied if the distribution of the colour polymorphic tawny owl (Strix aluco) morphs (a pheomelanic brown and a pale grey) across Europe follow the predictions of Gloger's rule and if there is a temporal change in the geographical patterns corresponding to regional variations in climate change. We used data on tawny owl museum skin specimen collections. First, we investigated long-term spatiotemporal variation in the probability of observing the colour morphs in different climate zones. Second, we studied if the probability of observing the colour morphs was associated with general climatic conditions. Third, we studied if weather fluctuations prior to the finding year of an owl explain colour morph in each climate zone. The brown tawny owl morph was historically more common than the grey morph in every studied climate zone. Over time, the brown morph has become rarer in the temperate and Mediterranean zone, whereas it has first become rarer but then again more common in the boreal zone. Based on general climatic conditions, winter and summer temperatures were positively and negatively associated with the proportion of brown morph, respectively. Winter precipitation was negatively associated with the proportion of brown morph. The effects of 5-year means of weather on the probability to observe a brown morph differed between climate zones, indicating region-dependent effect of climate change and weather on tawny owl colouration. To conclude, tawny owl colouration does not explicitly follow Gloger's rule, implying a time and space-dependent complex system shaped by many factors. We provide novel insights into how the geographic distribution of pheomelanin-based colour polymorphism is changing.

Melanin-based plumage coloration is associated with exposure in tawny owls under novel conditions

Intraspecific color variation is often associated with camouflage or protection, but melanin-based color variation is also linked to behavioral and physiological aspects including boldness. In the melanin-based plumage color polymorphic tawny owl (Strix aluco), the grey morph is known to be more cryptic than the brown morph. Using 19 captive tawny owls (11 grey and 8 brown), we tested if these two color morphs that differ in camouflage tend to differently use exposed perches in a familiar environment (home aviary) and a novel environment (experimental aviary), as well as whether their response to predation risk and mobbing cues differs. The two color morphs did not differ in their exposure under known conditions (in their home aviary), but brown tawny owls were more likely to use exposed perches than grey tawny owls after release in a novel environment.Significance statementMelanin-based coloration can be associated with several behavioral traits. However, it is still unknown how predators with genetically-based color polymorphism vary in their efficiency of active background choice and risk-prone behavior while facing predation risk or mobbing harassment. Using captive tawny owls, we investigated predators’ behavior (attention towards the stimulus and use of space) while confronted to mobbing events and predation risk. We showed that tawny owls were using their space differently according to their color morph in a novel environment (experimental aviary) but not in a familiar environment (home aviary).

Brown and grey morphs differ in their nocturnality in the polymorphic scops owl (Otus scops)

Detectability of morphs in different light environments is one of the mechanisms favoring the persistence of color polymorphism via disruptive selection. This mechanism predicts that different morphs should be more active and successful when light conditions make them more cryptic. In nocturnal birds, no study has analyzed yet whether morphs show a different degree of nocturnality, showing different circadian activity rhythms in relation to night and day light. We analyze activity patterns and hunting efficiency of color morphs in relation to day/night light in the nocturnal polymorphic scops owl (Otus scops). Forty-four percent of owl activity took place in the first hours after sunrise and before sunset. Also, we found that nocturnal activity decreased from grey to brown females and that grey males fed their chicks more than brown ones at night. Visual modeling revealed that grey individuals would be more conspicuous to their prey than brownish ones during the day. These findings suggest that part of the activity of nocturnal scops owls may occur during the day and that grey individuals would be better adapted to forage during night-light than brownish ones. However, brown morphs seemed not to be better adapted to forage at day, suggesting that other mechanisms than visual detection by predators or prey contribute to the persistence of color polymorphism in the species.Significance statementCircadian activity patterns can vary intraspecifically in response to changing environmental conditions. Color variants in polymorphic species could change their circadian activity rhythms differently in relation to diel luminal variation, switching from nocturnality to diurnality or vice versa, to achieve better background matching. We study for the first time whether different color variants of the nocturnal polymorphic scops owl (Otus scops) show different circadian activity rhythms with respect to night and day light conditions by relying on GPS-tracking data and nest video recordings. We also use perceptual visual modeling to study crypsis of morphs during the day. We found that nearly half of the activity of owls took place in the first hours after sunrise and before sunset. Also, we found that grey individuals would be better adapted to forage during night-light than more brownish ones probably due to their poor background matching during the day for the visual system of insects. These results support the idea that in scops owls, color morphs may show different degree of nocturnality to improve their crypsis.

Record of Onomarchus uninotatus (Serville, 1838) (Orthoptera, Tettigoniidae) as a pest of jackfruit from Kerala, India

Onomarchus uninotatus (Orthoptera, Tettigoniidae), one of the neotropical Pseudophyllinae is recorded on the jackfruit (Artocarpus heterophyllus) var. Vietnam Super Early at Thrissur, Kerala, India. This is a new distributional report of the species from Kerala and additional new documentation as a serious pest of jackfruit from India. The nymphs and adults are nocturnal in habit and feed on the leaves resulting in withering and drying of the leaves giving a burned up appearance to the canopy. The species exhibited colour polyphenism with green and brown morphs in the nymphal stages. A detailed description of the nature of damage caused by the pest is given.

Sex and Body Colour Affect the Variation in Internal Body Temperature of Oedaleus decorus asiaticus in Natural Habitats in Inner Mongolia, China

Oedaleus decorus asiaticus is one of the most harmful locusts in agricultural and pastoral areas in China. Plagues of this grasshopper can aggravate grassland degradation and cause huge damage to the livestock industry. Fungal biopesticides are seen as a suitable means of controlling grasshoppers and locusts. However, the efficiency of fungal biopesticides is dependent on temperature. Currently, there is limited knowledge on the thermal biology of this grasshopper in natural habitats. In this study, ground temperature measurements were made in conjunction with measurements of internal body temperatures using thermocouples and hand-held thermometers. The grasshoppers were randomly caught during the daytime in 2017 and 2018 in eight different locations in Inner Mongolia Autonomous Region, China. Our results indicated that the average internal body temperature of nymphs as well as adults of O. d. asiaticusis was higher than the ground temperature and that it increases/decreases with increases/decreases in ground temperature, respectively, during the daytime. Moreover, the adult internal body temperature is significantly higher than that of the nymphs at different times of the day, specifically around 6:00, 10:00, 13:00, and 18:00. Female internal body temperatures were significantly higher than those of the males by an average of 0.90 °C. Additionally, the average internal body temperature of the brown morphs was higher than that of the green morphs by approximately 1.17 °C. These findings demonstrate that brown morph insects might be more tolerant of fungal biopesticides and hence the biopesticides may take longer to kill them. Hence, ecophysiological adaptations to climate change may affect how fungal biopesticides could be used in the future.

Differentiation within the Drawida ghilarovi complex (Moniligastridae: Annelida) revealed by multigene transcriptomic dataset analysis

Drawida ghilarovi is an earthworm species with the northernmost distribution of all Monilidastridae in Asia. It includes multiple color morphs and has significant genetic diversity. In this study we used transcriptome sequencing to demonstrate that D. ghilarovi consists of three genetic clades that differ on both mitochondrial and nuclear genome levels. Pigmentation in D. ghilarovi appears to be labile, with frequent switching between different morphs. One of the clades of the complex is known from grey morphs only, the other consists of both grey and brown morphs, and the third one also has populations with black pigmentation. Two of the three clades are found only in the very south of the Russian Far East, while the third one has a distribution area that extends 800 km to the north, with the northernmost part of the distribution occupied by the black morph. We demonstrated that it would be phylogenetically unreasonable to divide the complex according to pigmentation, but splitting it according to genetic clades could be sensible.

No Wolbachia infection was detected in Drosophila elegans collected from the wild in the Ryukyu Islands, Japan.

Flower breeding, tropical and subtropical Drosophila elegans is distributed in the Ryukyu Islands and Taiwan (black morph) and in southern China, Philippines, Indonesia, and New Guinea (brown morph). Although reproductive and behavioral manipulations by Wolbachia are reported in many insect taxa, Wolbachia infection in D. elegans is unclear. There is only a report of no Wolbachia detected in a laboratory strain of brown morph. This PCR diagnosis study revealed no Wolbachia infection in D. elegans males collected from the wild in the Ryukyu Islands. We concluded that D. elegans black morph in the Ryukyu Islands is not infected with Wolbachia .

The weaker sex: Male lingcod (Ophiodon elongatus) with blue color polymorphism are more burdened by parasites than are other sex-color combinations.

The unusual blue color polymorphism of lingcod (Ophiodon elongatus) is the subject of much speculation but little empirical research; ~20% of lingcod individuals exhibit this striking blue color morph, which is discrete from and found within the same populations as the more common brown morph. In other species, color polymorphisms are intimately linked with host–parasite interactions, which led us to ask whether blue coloration in lingcod might be associated with parasitism, either as cause or effect. To test how color and parasitism are related in this host species, we performed parasitological dissection of 89 lingcod individuals collected across more than 26 degrees of latitude from Alaska, Washington, and California, USA. We found that male lingcod carried 1.89 times more parasites if they were blue than if they were brown, whereas there was no difference in parasite burden between blue and brown female lingcod. Blue individuals of both sexes had lower hepatosomatic index (i.e., relative liver weight) values than did brown individuals, indicating that blueness is associated with poor body condition. The immune systems of male vertebrates are typically less effective than those of females, due to the immunocompromising properties of male sex hormones; this might explain why blueness is associated with elevated parasite burdens in males but not in females. What remains to be determined is whether parasites induce physiological damage that produces blueness or if both blue coloration and parasite burden are driven by some unmeasured variable, such as starvation. Although our study cannot discriminate between these possibilities, our data suggest that the immune system could be involved in the blue color polymorphism–an exciting jumping-off point for future research to definitively identify the cause of lingcod blueness and a hint that immunocompetence and parasitism may play a role in lingcod population dynamics.

Cold winters have morph-specific effects on natal dispersal distance in a wild raptor.

Dispersal is a key process with crucial implications in spatial distribution, density, and genetic structure of species’ populations. Dispersal strategies can vary according to both individual and environmental features, but putative phenotype-by-environment interactions have rarely been accounted for. Melanin-based color polymorphism is a phenotypic trait associated with specific behavioral and physiological profiles and is, therefore, a good candidate trait to study dispersal tactics in different environments. Here, using a 40 years dataset of a population of color polymorphic tawny owls (Strix aluco), we investigated natal dispersal distance of recruiting gray and pheomelanic reddish-brown (hereafter brown) color morphs in relation to post-fledging winter temperature and individual characteristics. Because morphs are differently sensitive to cold winters, we predicted that morphs’ natal dispersal distances vary according to winter conditions. Winter temperature did not affect the proportion of brown (or gray) among recruits. We found that dispersal distances correlate with winter temperature in an opposite manner in the two morphs. Although the gray morph undertakes larger movements in harsher conditions, likely because it copes better with winter severity, the brown morph disperses shorter distances when winters are harsher. We discuss this morph-specific natal dispersal pattern in the context of competition for territories between morphs and in terms of costs and benefits of these alternative strategies. Our results stress the importance of considering the interaction between phenotype and environment to fully disentangle dispersal movement patterns and provide further evidence that climate affects the behavior and local distribution of this species.

Decline of the Commercially Attractive White Morph in Goliath Beetle Polymorphic Populations

The Goliath beetle (Goliathus goliatus) is one of the largest and most commercially valuable (for collection exports) beetle species worldwide, and occurs in West and Central Africa, with polymorphic populations being found in Benin, Eastern Nigeria, and Western Cameroun. The white morph is the most commercially valuable, and therefore is actively searched for by hunters and dealers. In a long-term, opportunistically conducted study in south-eastern Nigeria, we documented a substantial decline of the white morph compared to the normally coloured brown morph, although an overall decline in the number of observed beetles was evident for both colour morphs. Although a combination of reasons may have caused the white form decline, it is likely that overcollecting was the primary threat behind the observed pattern. Therefore, we urge the competent authorities to better protect the polymorphic populations of these giant beetles and the International Union for the Conservation of Nature (IUCN) to make a quick assessment for eventual inclusion of the species among the threatened taxa Red List.

Revision of the Asian pseudoscorpion genus Tullgrenius Chamberlin, 1933 (Pseudoscorpiones: Atemnidae: Miratemninae), a tale of intraspecific variation

The Asian pseudoscorpion genus Tullgrenius Chamberlin, 1933 is revised. A neotype is designated for Tullgrenius indicus Chamberlin, 1933, based on topotype material and a detailed description of its male is provided. Two new synonymies are proposed: Tullgrenius vachoni Murthy, 1962 syn. nov. and Tullgrenius orientalis Sivaraman, 1980 syn. nov. = T. indicus. Two distinct colour morphs of T. indicus are recognized: a brown and black morph. Supplementary descriptions and illustrations for Tullgrenius afghanicus Beier, 1959 and Tullgrenius compactus Beier, 1951 are detailed with current distribution of all the known Tullgrenius spp..

Significance of plumage colour for winter survival in the Tawny Owl (Strix aluco): revisiting the camouflage hypothesis

In snowy winters, the survival of Tawny Owls Strix aluco of the grey colour morph is suggested to be better than that of the brown (or red) morph, partly due to their paler plumage, which is presumed to provide better camouflage against predation. If the difference in the susceptibility to predation between the colour morphs is significant, this should probably be reflected in the relation between the number of snow‐covered days (i.e. the length of the winter) and the number and survival of owls of different colour. In a population in southern Finland there were no significant associations between the number of snowy days during winter and the number of breeding Tawny Owls of different colour morphs in the following spring, but the number of owls, in particular red ones, varied inversely with the number of snowy days in the winter of the previous year. The time lag suggests that the number of snow‐covered days (or some related factors) primarily influenced the pre‐breeding survival of young red owls. However, I found no effect of snow days on the proportion of colour morphs, suggesting only small differences in morph‐specific survival under long‐lasting winter conditions.

Does plumage colour signal fitness in the tawny owl Strix aluco?

Plumage colour has been hypothesized to signal fitness in its component parts survival and reproduction. In the tawny owl Strix aluco, grey individuals have been considered to be more viable and productive than brown ones in cold environmental conditions. The recent increase in the frequency of the brown morph in Finland has been explained by the climate warming. However, in recent decades there have been no trends in the general mildness of winters. Therefore, trends in the abundance of owls due to climate warming per se were unexpected. In a population near the southern coast of Finland, the abundance of grey (not brown) individuals increased significantly during the period 1986–2018, suggesting that natural selection has recently favoured the grey colour morph. During snowy and cold winters grey owls seemed to survive better than brown ones, suggesting that plumage colour signals adaptations to winter weather. The proportion of brown individuals in each year was best explained by the joint effect of snow cover and winter temperature. Extreme peaks in snow fall and cold winters seemed to affect substantially and rather similarly the abundance of both colour morphs. Between population differences in the occurrence of colour morphs were probably due to local and temporal differences in the snow cover. The number of fledglings was significantly related to the colour morph and weather conditions of the preceding winter in males but not in females. This suggests that coloration of males signals fitness in reproduction.

Specialist predation covaries with colour polymorphism in tawny owls

Understanding intraspecific phenotypic variation in prey specialisation can help to predict how long-term changes in prey availability affect the viability of these phenotypes and their persistence. Generalists are favoured when the main food resources are unpredictable compared to specialists, which track the availability of the main prey and are more vulnerable to changes in the main food resource. Intraspecific heritable melanin-based colour polymorphism is considered to reflect adaptations to different environments. We studied colour morph-specific diet specialisation in a generalist predator, tawny owl (Strix aluco), during offspring food provisioning in relation to mammal prey density. We hypothesised that the grey morph, with higher fitness than the brown in Northern boreal conditions, is more specialised in mammalian prey than the brown morph, which in turn has higher fitness than the grey in the temperate zone. We found a higher diversity of prey delivered to the nest by brown fathers compared to grey ones, which also depended on the overall mammalian prey availability. Brown fathers provided proportionally fewer mammalian prey than grey in poor, but not in favourable mammal prey years. Our results suggest that the brown morph is more generalistic and reacts more strongly to variations in food supply than the grey morph, which may be a beneficial strategy in an unpredictable environment caused by environmental degradation.Significance statementDiet choice of a species may vary depending on fluctuations in the abundance of their food resource, but also within a population, there can be adaptations to use different food resources. The tawny owl exhibits a grey and a reddish-brown colour morph and is considered a generalist predator eating both mammal and bird prey. We find that the diet of the reddish-brown morph is more diverse than that of the grey. When the tawny owls’ main prey, small mammals, are abundant both colour morphs prey on mammals, but in years with less small mammals, the reddish-brown morph is more prone of switching to small bird predation than the grey. The generalist strategy of the brown morph is likely to be more favourable than a stricter specialisation in small mammals of the grey under recently reoccurring irregularities in small mammal dynamics.

Where one species leads, another follows: interspecies processions in tropical caterpillars.

One sunny July morning on the Neotropical island of Trinidad, a group of caterpillars, hundreds strong, marched in head-to-tail procession up their host tree. Among them were two morphs: the majority, long-haired and black, and in smaller numbers, a more cryptic short-haired brown morph. Both proceeded up the tree trunk, thoroughly integrated, and indistinguishable from each other in their behavior. At the bifurcations of branches they split into smaller processions, and continued to the very tips of the branches.

ЭЛЕМЕНТНЫЙ СОСТАВ ГОНАД, ПОЛОВЫХ ПРОДУКТОВ И ЛИЧИНОК ЧЕРНОЙ И КОРИЧНЕВОЙ МОРФ ДВУСТВОРЧАТОГО МОЛЛЮСКА MYTILUS GALLOPROVINCIALIS LAM.

Concentrations of the bulk and trace elements were determined in male and female gonads, gametes (sperm and eggs), and larvae (trochophores) of black and brown morphs of the Mediterranean mussel Mytilus galloprovincialis using energy dispersive X-ray spectroscopy and inductively coupled plasma mass spectrometry. The mollusks were collected in spring 2019 on a mussel-and-oyster farm (Black Sea, Crimea, Sevastopol, Karantinnaya Bay). In the male and female gonads of black and brown morphs, no statistically significant differences were detected in concentrations of the bulk structural elements (C, N, O, P, S), while in gametes and trochophores, these differences were significant. Trace elemental analysis revealed that in the female gonads of both black and brown morphs, Cu, Fe, and As were dominant, however in brown morphs, concentrations of these elements were significantly lower than in black mussels. Zn and Se concentrations in the gonads of black morphs were significantly higher than in brown mussels. Most of the statistically significant differences were found between trochophores and eggs of black vs. brown morphs. These data show that the two M. galloprovincialis morphs differ in their elemental composition.