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Proteomic explanations for the adaptive significance of kin recognition in subsocial spiders

Final Report Summary - PROKIN (Proteomic explanations for the adaptive significance of kin recognition in subsocial spiders)

Kin selection theory predicts that cooperation should evolve among kin to reduce the costs of helping and the incentive to cheat. Altruistic behaviour provides individuals with either direct or indirect fitness benefits. As a necessary prerequisite, individuals need to recognise kin to direct their help towards them. Thus, kin recognition is a key feature of many social animals. Although the ultimate benefits of altruism are well studied, the proximate mechanisms explaining maintenance and evolution of kin recognition as the mediator are still poorly understood.
This project investigated the adaptive significance and the mechanisms of kin recognition in subsocial Stegodyphus spiders (Araneae, Erisidae). These animals provide an excellent model system as the genus comprises species with solitary living over temporary group living (subsocial systems) to permanent formation of social groups. The complexity of social interactions is less pronounced than that of eusocial insects. However, social Stegodyphus spiders cooperate in web building (including nest construction), hunting and feeding. This cooperation, and especially the communal foraging, increases the individual chance of survival to the reproductive stage, but may be associated with the cost of an increased inbreeding risk. In subsocial species this risk is eliminated by a pre-mating dispersal. After cooperating over several instars the spiders leave the communal nest as late juveniles and enter a solitary life stage in which they grow to adulthood.
With respect to intra-individual communication, the ability to recognise kin has only been revealed for subsocial species but it lacks in permanently social species. It has been proposed that kin recognition leads to a preferential association with kin which facilitates the evolution towards permanent sociality where spider colonies are formed out of family bonding with an inbred mating system, overlapping generations within nests and life-time cooperation. The rare encounter with unrelated individuals may then have led to a loss of kin recognition as result of a relaxed selection pressure. However, it is still unclear what maintains kin recognition in the subsocial species? A few studies showed that a preferential association with related individuals increases the efficiency of cooperation. In particular, spiders in groups of only siblings grow faster and bigger than those in mixed kin groups. The sheer existence of the latter illustrates the difficulties to understand the maintenance of kin recognition in these spiders. Because behavioural experiments showed very low aggression levels between kin and non-kin individuals. Unrelated individuals are readily accepted to groups and cooperate with their members.
We here particularly studied two subsocial spider species Stegodyphus lineatus (from Israel) and Stegodyphus africanus (from South Africa). Previous studies found a lack of discrimination against unrelated individuals, and non-kin groups of spiders do also cooperate. We were specifically interested why and how kin recognition is maintained in those spiders if they do not use this ability to discriminate against unrelated individuals. And, we aimed to reveal that the key of understanding the adaptive significance of kin recognition resides in a kin-specific investment in extra oral digestion (EOD) when these spiders feed communally. We predicted that competition among unrelated spiders exists, perhaps in a very subtle way or taking place even at the digestion level. Like other spiders Stegodyphus releases digestive fluids onto or into the body of captured prey to dissolve its tissues before consumption. In group feeding events of subsocial and social species several or all spiders will participate in EOD. However, this allows for different scenarios in which the efficiency of the digestion can be impaired by completion among individuals based on their relatedness. The benefits of cooperation may be reduced by molecular incompatibilities of enzymes of unrelated spiders, by subtle behaviours to try to prevent unrelated individuals from feeding or by a greater tendency to not participate in the digestive fluid release while feeding with non-kin. Thus, we hypothesised that the previously observed difference in feeding efficiency between kin- and non-kin-groups derive from either subtle competition depending on the relatedness of co-foragers or compatibility problems of enzymes of unrelated individuals.
We used a combined approach using proteomic analyses, in-vitro digestion and behavioural experiments on our study species S. lineatus. Proteomics were used to 1) reveal the enzymatic composition of digestive fluids, 2) to check for nest-specific protein-profiles (relatedness) and 3) to identify candidate enzymes that could be used for quantitative proteomics. In addition to that we conducted feeding experiments where we manipulated the relatedness of spider group members and investigated their feeding behaviour and efficiency in close detail. For the latter experiment we needed to introduce a second Stegodyphus species to our research plan as we experienced housing and breeding difficulties with S. lineatus in the lab. For the behavioural experiments we used S. africanus, another subsocial species from South Africa.

We found no specific differences in the enzymatic composition of digestive fluids among S. lineatus spider nests that might explain differences EOD effectiveness based on kin-related incompatibilities of released enzymes. Proteomic analyses revealed highly variable protein compositions of digestive fluids. Accordingly, the individual protein-composition of digestive fluids of communally feeding spiders is highly diverse, creating an infinite number of potential mixtures when a number of spiders feeds together. Hence, it is very unlikely that incompatibilities can produce the highly predictable pattern of better performance in kin-group feedings. Based on the same results we could also not detect candidate enzymes that might have been overrepresented in the fluids and possibly used for quantitative proteomic analyses. With labelling those candidates and tracking their relative amount inside the prey’s body we were hoping for estimating the relative contribution of each spider in a feeding group.
In in-vitro digestion experiments we then aimed to circumvent the uncertainty about specific proteins in digestive fluids and directly test the digestion efficiencies of mixtures of fluids of unrelated individuals. Using pre-defined amounts in a mix we showed that, brought together, digestive fluids of kin and non-kin individuals do not reduce the decomposition rate of prey tissues compared to a mix obtained from related individuals only. However, this experiment has not been completely finished and it has to be shown if further fine-tuning of prey tissue and enzyme concentration as well as digestion time cannot still reveal some digestion efficiency differences.
Finally, our behavioural studies on S. africanus firstly confirmed that group feeding is significantly more efficient in kin groups. Yet for the first time we could show how this is the result of competitive behaviours among the co-foraging spiders. We setup feeding groups of six spiders either consisting of full siblings (same nest) or cross-fostered unrelated individuals (that grew up in the same nest, but came from two different mother nests) and conducted 200 individuals feeding trials. In the weeks prior to the trials neither aggression nor cannibalism was recordable in the mixed kin groups and the spiderlings cooperated in the typical way, like it was observed in earlier studies. However, when the prey (houseflies) was introduced to the petri dishes containing the test groups the attack time was significantly delayed in the mixed kin treatment. In fact, in groups of unrelated spiders it takes twice as long for the first individuals to attack the prey. After a few minutes the first spiders would then start to bite the body of the prey and start the actual feeding, by releasing the digestive fluids. In mixed groups significantly fewer individuals participated in the feeding. This observation is not the result of a lower motivation of spiders to feed but rather the result of a higher probability of the spiders wrangling over the prey. In mixed groups individuals more frequently tried to monopolise the prey items and tried to chase co-foragers off. These behaviours did not escalate to serious fights among individuals, but it significantly reduced the amount of prey biomass ingested over time. By measuring the body mass change of the prey over time we found that in kin groups the presented houseflies started to significantly lose mass 16min into the feeding trial, on average four minutes earlier than in the mixed groups. In combination, these result indicate a reduce efficiency of prey capture and feeding in groups of genetically unrelated individuals. Two hours after the feeding trial has started significantly less prey biomass was consequently extracted in mixed kin groups.

In conclusion, we found no evidence for molecular incompatibilities of digestive enzymes between kin and non-kin individuals in Stegodyphus lineatus. Our results on S. africanus rather suggest that kin recognition in subsocial Stegodyphus spiders is maintained to adjust the individual contribution to group foraging, with a reduced investment if spiders hunt and feed together with non-kin. Overall aggression is low but subtle competition is measurable, and significant, when it comes to foraging. From an evolutionary perspective this result is conceivable, as it is beneficial to allow foreign individuals to join groups in order to generally increase foraging efficiency. It reduces per capita costs for web building and individual mortality (due to predation and injuries while attacking prey). Thus, it increases the probability of capturing large prey items and/or more prey items in succession. However, as soon as the feeding started selfish motivations result in competitive behaviours that counteract the positive group size effects. Subsocial Stegodyphus spiders have to master the delicate balance between the need for cooperation and drive for selfish fitness gain. Inclusive fitness theory predicts lower degrees of competition among related individuals. Hence, we suggest that the adaptive value of kin recognition in these spiders resides in reducing competition and thereby increasing foraging efficiency by a preferential association with kin.