Theridion grallator, also known as the Hawaiian happy-face spider, is a spider in the family Theridiidae that resides on the Hawaiian Islands. T. grallator gets its vernacular name of "Hawaiian happy-face spider" from the unique patterns superimposed on its abdomen, specifically those that resemble a smiley face. T. grallator is particularly notable because of its wide range of polymorphisms that may be studied to allow a better understanding of evolutionary mechanisms. In addition to the variety of color polymorphisms present, T. grallator demonstrates the interesting quality of diet-induced color change, in which its appearance temporarily changes as it metabolizes various food items.
Description
T. grallator is a small spider with a body size less than 5 millimeters long. It has characteristically long and slender legs and a translucent yellow body. These distinctly long legs lead T. grallator to have the most divergent bodily morphology out of all the members of its clade. This unique characteristic occurred as a result of an ecological or behavioral shift.
Its abdomen is often pale, translucent yellow, and can also contain a variety of red, white, and/or black superimposed patterns. Certain morphs have a pattern resembling a smiley face or a grinning clown face on their yellow body, hence their vernacular name. These patterns differ from island to island. Some lack abdominal markings altogether. Abdominal color changes from translucent yellow to green or orange, depending on diet. The variety of polymorphisms present in T. grallator allows an evolutionary benefit to evade predation. Spiders with depigmentation or polymorphic colors and patterns can avoid predation by birds that use a search image when scanning for prey. A search image may be a particularly abundant color morph, and predators will use this as an identification of possible prey.
Color morphs A key characteristic of T. grallator is the presence of a large variety of abdominal color morphs. The ratio of unpatterned to patterned morphs is relatively constant throughout the year. It is also constant between and within populations regardless of climate and elevation, indicating some form of selection acting to maintain these proportions. Although across all of the Hawaiian islands, there is a similar frequency of the discrete morphs, there are different genetic bases for these morphs between islands. The various morphs are assigned to a series of broad categories that characterize the abdominal color and/or its patterned patches. These categories include: Yellow, Red front, Red back, Red front and back, Red lines, Red ring, Black ring, Red/black ring, Red blob, Red/black blob, and White.
Genetic factors underlying color morphs These color polymorphisms follow simple Mendelian genetics. The most common morph is Yellow, which makes up 70% of populations. Genetic studies of these morphs have shown that the Yellow morph, which is also known as the "unpatterned" morph, is recessive to all patterned morphs. Within patterned morphs, the amount of pigment present in the abdomen is correlated with the dominance of the associated allele. The alleles that are associated with black, red, or white pigments are arranged in a hierarchical structure and exhibit dominant effects. In addition, unpatterned morphs are recessive to patterned morphs. Lastly, White is dominant to nearly all morphs. The White morph is produced by a massive deposit of guanine below the hypodermis, a structure derived from the ectoderm. The presence of this white background is beneficial when bright-colored morphs are advantageous. Guanine is the main nitrogenous excretory product in spiders. These deposits create a white background between the brown digestive diverticula, a structure of the midgut, and the hypodermis. These guanine deposits and their distribution within the body are under the control of a major gene loci in T. grallator. This major gene loci is under the control of two mechanisms. These two mechanisms respond to the presence or absence of guanine and send chemical signals between the hypodermis and digestive diverticula to adjust morph pigmentation. In addition, these two mechanisms may function independently or together. The first mechanism operates by inhibiting the effect of guanine on pigmentation; thus, unpigmented areas will contain a layer of guanine beneath. The second mechanism operates by inducing guanine with light, resulting in guanine deposits present under unpigmented areas. Guanine is found only under the red and black hypodermal pigments that form the various morph patterns. White and Red lines exhibit codominance. There appears to be no sex-linkage in the distribution of morphs between sexes.
Theridion grallator is known for its exuberant carapace and opisthosoma (abdomen) patterning. Opisthosomal morphs appear to be dictated by alleles at one autosomal locus. Dominance typically comes from superimposing one pattern over the other. The linkage between loci may be responsible for the association between carapace and opisthosomal patterns. Although there is a possibility of pleiotropic effects of alleles at one particular locus, it is not likely given the associated patterning on the carapace and abdomen. One example of this is the red and black opisthosoma pigmentation with guanine deposits, showing the benefit of the visual effects of these color polymorphisms.
Population structure, speciation, and phylogeny Close relatives At least nine species in the Hawaiian islands have been identified to be members of the T. grallator-clade based on the analysis of genitalia patterns. This clade is believed to have been colonized from the Americas and is closely related to the genus Exalbidion. The closest relatives of T. grallator are other Hawaiian species, such as Theridion posticatum, Theridion kauaiense, and Theridion californicum. In T. grallator as well as T. californicum, there is one inconspicuous morph (namely, Yellow in T. grallator) that is the most common and an assortment of less common and seemingly more conspicuous morphs. This "T. grallator clade" may be more closely related to the genus Exalbidion than to any other species currently classified in the genus Theridion. Molecular clock data estimates that T. grallator first diverged from its ancestors about 4.22 Ma.
Most of the Hawaiian Theridion are believed to be closely related except for T. actitarase, which contains a number of common traits with the related Rugathodes genus. Similar traits include the palpal organ and certain genitalia features. There is another Theridion species, which remains unnamed, that also displays features that are distinct from most Hawaiian Theridion. However, this unnamed species does contain a few characteristics that resemble the T. grallator, namely, its long legs and abdominal shape. Thus, this unnamed Theridion species may have evolved under similar evolutionary pressures as T. grallator. Despite some variations in the bodily appearance of the Theridion species, there still remains a uniformity in sexual behavior. There is also a highly uniform web-building behavior and structure. There has been much debate on how to organize clades and construct an appropriate phylogenetic structure of Theridiidae, and work is still being done to properly classify these species.
Genetic population structure The genetic bases of the abdominal color morphs of the T. grallator vary by island despite the actual abdominal color morphs having an identical appearance throughout the islands. On Maui, the color morphs of T. grallator originated from one locus while those on Hawai’i have at least two unlinked loci involved in the color polymorphisms. In addition, on Maui, all polymorphisms are attributed to individual alleles while on Hawai’i, there are two pairs of color morphs that may depend on one single locus that is differentially expressed in males and females. One pair of these differentially expressed morphs is the Yellow and Red fronts, where the morph manifests phenotypically as Yellow in females but Red in males. Similarly, the Red blob and Red ring in Hawai’i populations have a varied manifestation between the sexes with the Red blob in females and Red ring in males. These differences in phenotypes are most likely due to differential expression and not sex-linkage.
The different genetic backgrounds in the color morphs of T. grallator in Maui and Hawai’i are due to the difference in ages of the two islands and their colonization. Maui emerged first, followed by Hawai’i. Because of the presence of some sex-selective morphs in Hawai’i - a phenomenon not observed in Maui - it is likely that a shift in inheritance pattern occurred due to evolutionary pressures. Currently, there is very little exchange of individuals amongst the Hawaiian islands, as shown by the distinct formation of monophyletic clades on each island. Despite the difference in genetic backgrounds and the rare exchange of individuals, hybrid matings between islands can still produce viable offspring. This indicaties that T. grallator on Maui and Hawai’i are not too differentiated from one another.
Evolution and selection The evolutionary significance of the color polymorphisms of T. grallator is elusive, but there are selection pressures acting on the various morph proportions. The Yellow morph sometimes exists in proportions of about 70% of the total population. The remaining portion of the population displays a variety of the patterned morphs. This high skew toward the Yellow morph indicates that there must be evolutionary significance involved in this specific polymorphism. The predominant theory to explain this skew is predator selection. Because T. grallator resides on the underside of green leaves, the Yellow morph provides them a degree of conspicuousness under the sunlight. This allows them to better evade predators. However, there still exist advantages to the other color polymorphisms despite their lower observed frequencies. This can also be explained in terms of predation. Females benefit much more from the Yellow morph because they are largely sedentary, residing on their leaves most of the time. The male T. grallator is much more mobile and spends much of its time on the ground, searching for mates. Without the shield of the leaf, the Yellow morph will not always be the most beneficial to males; some rarer patterned morphs provide an increased level of conspicuousness and thus allow these males to evade predators. Thus, when the Yellow morph reaches a frequency higher than normal, the Yellow morph females may shift their preference to these conspicuously patterned males. Until this patterned morph no longer provides an advantage from predators, females will continue to place their preference on these patterned morphs.
The mosaic nature of Hawaiian the islands has allowed for the differentiation of adaptive color variations and polymorphisms. At the younger sites, there is less genetic diversity and the older locations have a much higher diversity of haplotypes.
Habitat and distribution
Habitat T. grallator inhabits wet and mesic environments. Wet environments are defined as having an annual rainfall from 200 to 350 centimeters and mesic environments are defined as having an annual rainfall of 100 to 200 centimeters. These spiders are found in the forests of the Hawaiian Islands. They have been found on the islands of O’ahu, Moloka’i, Maui, and Hawai’i. They prefer to reside on the underside of plant leaves such as the native Broussaisia arguta and Clermontia arborescens and the introduced Hedychium coronarium. H. coronarium is a particularly tactical plant to reside on as its large, slippery leaves allow T. grallator to better evade predation.
These spiders have been seen in kipukas, areas that have been surrounded by lava flows. However, they are not found in the lava flows surrounding the area.
Geographic distribution