Evolution of Sociality: mechanisms and dynamics of social behavior in spiders

Most animals live solitarily, but for some species the benefits of group living outweigh the costs and social communities have evolved. Truly social societies are characterized by cooperation in tasks like foraging, predator defense and brood care. In the most extreme cases, non-reproducing individuals act as helpers and provision offspring of reproducing individuals at the cost of their own reproductive success. This alloparental care is attributed to kin selection that provides the helpers with inclusive fitness benefits. However, how reproductive role is determined and in which ways virgin helpers in a group benefit the community is not always well understood. Spiders are known to be generalist hunters, which in many cases do not shy away from cannibalism. Thus, most spiders live solitarily. However, in a few species a permanently social lifestyle has evolved in which individuals live together throughout their life, providing an intriguing case of social evolution. These spider communities are characterized by lack of premating dispersal leading to extreme inbreeding, by reproductive skew, in which only a proportion of females reproduce and by cooperative breeding of the reproducing females. It has been assumed that the large proportion of virgin females act as helpers not only in foraging and web maintenance but also during brood care. In the social spider Stegodyphus dumicola brood care involves the intensive task of regurgitation feeding, at which mothers regurgitate their own liquefied body tissue. At the end of brood care, the offspring sucks the mothers dry during matriphagy, leading to the death of brood caring females and a semelparous lifestyle. In the closely related solitarily breeding Stegodyphus lineatus virgin females do not provide brood care. The ability of virgin females in S. dumicola to care for offspring would thus depict an adaptation to sociality and cooperative breeding. I therefore aimed to clarify the role and significance of virgin females in colonies of social spiders and furthermore investigated a possible mechanism of how reproductive role within a colony is determined. I investigated whether there is differential task participation in a non-reproductive task and the task of brood care among reproducing mothers and virgin females (helpers) in Stegodyphus dumicola. The study provides explicit evidence that brood care – including egg sac care, regurgitation feeding and matriphagy – is performed by mothers as well as by virgin helpers. Virgin females in a colony can thus rightfully be termed allomothers. However, the task participation differed between the reproductive states. While mothers engaged more often in brood care, virgin females were more active in foraging. However, the active provisioning of offspring by the virgin females decreases the motherly workload as is suggested by the extended brood care period in comparison to solitary breeders. The observations on virgin allomaternal care are supported by histological studies on the midgut tissue of brood caring females, which revealed that mothers and virgin helpers undergo comparable morphological changes in preparation of regurgitation feeding. The changes in virgin females correlate to ovarian development that might depict an internal maturation process which sets virgin females in the right state to provide care. The morphological changes in mothers and virgin helpers of S. dumicola are less comprehensive than in the solitarily breeding S. lineatus mothers. This indicates that cooperatively caring females are able to save on their resources, provision offspring for longer and thus are probably able to increase survival of the brood by an extended care period. A surprising consequence of cooperative brood care is the ability of mothers to produce a second viable egg sac, even when the first brood is successful. Mothers of the cooperative breeding S. dumicola can thus depart from the strictly semelparous lifestyle and instead invest part of their resources in a second clutch. This finding identified a new way of how cooperative breeding enhances breeding success of reproducers and thus inclusive fitness for helpers as well, thus adding to the benefits of allomaternal care. Virgin females did not store significantly lower amounts of lipids in their midgut tissue than mothers, raising the question of how much reproductive role of females is determined by competition for resources during growth, as often assumed. Another possible determinant of female reproductive skew is the characteristic male scarcity in spider colonies, with only about 12 percent of spiders being male. Males are assumed to mature early within a few days and die early, thus leaving late maturing females unmated due to lack of mating partners. However, my studies provided evidence that male maturation is more skewed than expected and males might survive several months. Subadult females did not accelerate molting when an adult male was present, which could further indicate, that male presence is not a limiting factor on reproduction in males. Furthermore, males are able copulate with up to 16 females and did not show e preference for large females during mating trials. Males are thus able to fertilize all females, provided all females mature in time. I therefore suggest, that male scarcity is not major determinant of reproductive skew in females, especially in small and middle-sized colonies in which female maturation might only be moderately skewed. My studies were able to demonstrate the meaning of the large proportion of unmated females in a colony of the social spider S. dumicola. Virgin helpers support mothers during brood care and thus do not only enhance the brood care period but facilitate mothers to produce multiple clutches. Virgin females are able to care as they undergo similar morphological changes as mothers’ do. This seems to be facilitated by an internal maturation process, indicated by ovarian development and oviposition by virgin females, both of which has never been observed in virgins of the subsocial species. How reproductive role is determined remains unclear, but I was able to exclude male scarcity as a major factor influencing reproductive skew.Dauerhaftes Zusammenleben in sozialen Gemeinschaften und Kooperation sind seltene Phänomene bei Spinnen, welche sonst als kannibalistische Einzelgänger gelten. Permanent sozial lebende Spinnen bilden damit eine geeignete Basis, um zu untersuchen, wie Sozialleben evolutionär entstanden ist und welche Mechanismen es bestimmen und steuern. Das intensive Brutpflegeverhalten der Spinnenweibchen gilt dabei als Schlüsselkomponente auf dem Weg zur Sozialität. Mit Hilfe morphologischer und verhaltensbiologischer Ansätze untersucht diese Arbeit das kooperative Brutpflegeverhalten der sozialen Spinne Stegodyphus dumicola und erörtert dabei insbesondere die Rolle virginer Weibchen bei der Jungenaufzucht. Die Ergebnisse der Studie tragen dazu bei die Evolution der Sozialität innerhalb der Spinnen und die aus der sozialen Lebensweise hervorgehenden Konzequenzen besser zu verstehen

Comparative female genital morphology in Stegodyphus spiders (Araneae: Eresidae)

The anatomy of the female genitalia sets the arena for sperm competition in species in which females mate multiply and store sperm. In spiders, females possess cuticular internal structures that have evolved into diverse sperm storage sites. Here, we investigate the female genital morphology of seven eresid spider species. We used X-ray micro-computed tomography for 3D reconstruction of the anatomy of the female genital system in the social Stegodyphus dumicola, S. mimosarum and S. sarasinorum, and the subsocial S lineatus, S. pacificus, S. tentoriicola as well as Eresus sandaliatus. We used histology to assess the sites of sperm storage in two selected species S. lineatus and S. dumicola. Our results show that the internal genitalia of the Stegodyphus species consist of two bilateral folds instead of closed ducts as often reported for entelegyne spiders. Along each fold, three regions are discriminable that differ in their specific morphology but are all surrounded by glandular tissue. Between species, the regions differ in shape and dimension. In virgin females, the lumina of all regions are filled with secretion. In mated females, spermatozoa were found in all three regions; however, only those sperm that are stored in the posterior region seem to become activated. Sperm found in anterior regions are embedded in a substance that might act as a mating plug. Our data suggest that the regions of the female genital tract differ in accessibility by the male as well as in their potential use for ejection and manipulation of sperm by the female. (C) 2018 Elsevier GmbH. All rights reserved

New distribution record of Bicolored Trailing Ant, Monomorium floricola (Jerdon, 1851) (Hymenoptera, Formicidae) from Ecuador, with information on cohabitation with the social spider Anelosimus eximius (Keyserling, 1884)

Invasive ant species are a serious threat to native fauna, especially in highly diverse tropical countries. Therefore, new distribution reports and information on the interactions with other species are essential to understand the potential effects of invasive ants on biodiversity. Here we report for the first time the presence of colonies of Monomorium floricola (Jerdon, 1851) in the nest of the Neotropical social spider Anelosimus eximius (Keyserling, 1884) in the southern part of the Ecuadorian Amazon. Our report extends the known distributional range of M. floricola to the southern Ecuador

In vitro studies to evaluate the wound healing properties of Calendula officinalis extracts

Ethnopharmacological relevance: Calendula officinalis (pot marigold) flower extracts have a long-lasting tradition in ethnopharmacology. Currently, the European Medicines Agency (EMA) has approved its lipophilic and aqueous alcoholic extracts as traditional medicinal products for the treatment of minor inflammation of the skin and as an aid in the healing of minor wounds. Aim of the study: The purpose of this study was to analyse the molecular mechanism of the wound healing effects of Calendula extracts, which may reflect the phytomedicines currently used in the market. Materials and methods: The effect of three different extracts from Calendula flowers (n-hexanic, ethanolic, aqueous) on the inflammatory phase of wound healing was studied in human immortalized keratinocytes and human dermal fibroblasts. An electrophoretic mobility shift assay on NF-κB-DNA binding, qRT-PCR and ELISA experiments were performed. The effect of Calendula extracts on the new tissue formation phase of wound healing was evaluated by studying the migratory properties of these extracts, triterpene mixtures and single compounds in human immortalized keratinocytes using the scratch assay. Finally, the effect of the extracts on the formation of granulation tissue in wound healing was studied using bacterial collagenase isolated from Clostridium histolyticum and the determination of soluble collagen in the supernatant of human dermal fibroblasts. Results: The n-hexanic and the ethanolic extracts from Calendula flowers influence the inflammatory phase by activating the transcription factor NF-κB and by increasing the amount of the chemokine IL-8, both at the transcriptional and protein level, in human immortalized keratinocytes. The migration of the keratinocytes during the new tissue formation phase was only marginally influenced in the scratch assay. However, it can be assumed that the granulation tissue was affected, as the ethanolic extract inhibited the activity of collagenase in vitro and enhanced the amount of collagen in the supernatant of human dermal fibroblasts. Conclusions: Our results contribute to a better understanding of the wound healing properties of the traditional medicinal plant Calendula officinalis. However, further studies are necessary to evaluate which of its known constituents are responsible for these effects. Triterpenes seem to play only a marginal role, but carotene and xanthophyll derivatives should garner more attention in future studies.UCR::Vicerrectoría de Investigación::Unidades de Investigación::Ciencias Básicas::Centro de Investigaciones en Productos Naturales (CIPRONA

Physiological Adaptations to Extreme Maternal and Allomaternal Care in Spiders

Some semelparous species show terminal investment by suicidal offspring provisioning. This requires internal cellular disintegration for the production of regurgitated food and in preparation for the sacrifice of the female body to the offspring, however, we have limited insights into the extent and costs of such physiological modifications. Extreme provisioning is hypothesized to be limited to reproducing individuals because it requires physiological alterations triggered by reproduction. However, non-reproducing helpers-at-the-nest have been shown to engage in suicidal provisioning, prompting us to ask whether helpers undergo similar physiological alterations to brood provisioning as mothers, which would represent an adaptation to cooperative breeding. Using an experimental approach, we investigated the physiological consequences of extended maternal care in the solitary spider Stegodyphus lineatus and the cooperative breeder S. dumicola, and whether non-reproducing helpers (virgin allomothers) in S. dumicola show physiological adaptations to brood provisioning. To identify costs of offspring provisioning, we determined the energy expenditure (standard metabolic rate; SMR) and tissue disintegration over the course of brood care. In both species, brood care is associated with elevated SMR, which was highest in allomothers. Brood care results in progressive disintegration of midgut tissue, which also occurred in allomothers. On experimental offspring removal, these responses are reversible but only until the onset of regurgitation feeding, marking a physiological “point-of-no-return.” The mechanism underlying the onset of physiological responses is unknown, but based on our finding of mature eggs in mothers and allomothers, as opposed to the undeveloped eggs in virgins of the solitary species, we propose that oocyte maturation is a central adaptation in non-reproducing helpers to provide terminal allomaternal care