Final Report Summary - INSSOCPLAS (Do nutritionally poor environments promote sociality? Testing a long-standing hypothesis in two socially plastic insect groups.)
Despite nearly fifty years of research and debate about the kinds of circumstances that favour social behaviour, there are still significant gaps in our understanding. Genetic circumstances that favour sociality were debated for decades, but poor environments may also make independent breeding difficult –driving individuals to stay at home and help relatives to breed. There is an important, long-standing but untested alternative, however. It may not be poor environments driving individuals to become social helpers, but poor individuals themselves; in particular, individuals that receive poor nutrition. This is called the “nutritional constraints hypothesis”. To test this, we need to perform nutritional manipulations in rare “socially plastic” species, i.e. those where individuals can choose to become social or solitary.
In the 24-month Outgoing phase, I aimed to test this hypothesis in a socially plastic species of thrips, Dunatothrips aneurae, endemic to the Australian Outback. D. aneurae build silken nests on a variety of Acacia tree in the arid interior of Australia, and some nests are cofounded – i.e. individuals decide to found nests individually or as groups. My objective questions were:
1. What is a “preferred diet” for Dunatothrips aneurae? Do nymphs raised on experimentally imbalanced diets tend to cooperate more readily as adults?
2. Is cooperation in the field correlated with the nutritional value of the plant?
3. Does manipulating the plant’s composition via fertilization affect cooperation in the insect?
4. Does nutritional imbalance affect the division of reproduction within a shared thrips nest?
I am in a position to answer at least one question, with another pending analysis. Two questions proved to be unfeasible to answer within the timeframe of the fellowship in the form I originally proposed. First, I have been able successfully to answer question (2) in the negative: there were no correlations between the nutritional content of the plant and cooperative behaviour in the thrips inhabiting the plant. Thus, using these correlational data I have been able to reject the nutritional constraints hypothesis for D. aneurae.
The complementary question (1), in which I planned to manipulate nutrition for nymphs using artificial diets, has been tricky to answer because of difficulties culturing nymphs in the laboratory. However, I have recently shown that these difficulties were largely due to the thrips’ requirements for high humidity – I have now published a paper demonstrating that the thrips’ nests function to reduce desiccation in the arid outback (Gilbert 2014). With this information, I am now able to plan further lab experiments at controlled, high humidity, but this will be outside the time frame of the fellowship and is a question for future research. I have, however, made progress towards answering this question by conducting a preliminary experiment to ask what a balanced artificial diet looks like for an adult Dunatothrips – I am still analysing the results. Question (3) proved similarly difficult to address, because my pilot studies showed convincingly that the nutritional composition of the Acacia trees do not respond at all to watering or fertilization! This is probably because they are extremely slow-growing and desert-adapted, and possibly also because they have a symbiotic relationship with nutrient-fixing microbes that may provide a buffer against environmental changes such as my manipulations.
To answer question (4) I am analyzing genetic relatedness from over 500 thrips and their offspring from more than 100 nests, having first established suitable microsatellites. This will provide a picture of the genetic structure on trees with different nutritional composition – and whether reproduction on nutrient-poor trees shows the predicted skew in favour of one female.
Since I was able to reject (tentatively) a nutritional explanation for cooperation in Dunatothrips, I conducted behavioural experiments and observations to investigate alternative bases for cooperation in this species. I have published a paper detailing the natural history of D. aneurae, which was previously poorly understood (Gilbert & Simpson 2013) as well as the biology of a new species of social parasite which I found living within their nests (Gilbert et al 2012). I have shown that D. aneurae are pacifists with no defence behaviour, so cooperation is not related to defence. Cooperation may partly be a response to local crowding on branches, as crowded nests are more cooperative. Accordingly, cooperation carries a cost because of competition for space in nests - some females in smaller nests are nonreproductive. These nonreproductive females tend not to help rebuild damaged nests, maybe because they have no genetic stake in offspring.
In summary, my results from the Outgoing phase have provided a rejection of a longstanding hypothesis about social evolution, at least in one species of socially plastic thrips – a valuable contribution to social biology. In addition, I have substantially helped understand D. aneurae biology by publishing (1) an account of its natural history, (2) the exciting discovery of humidity-controlled nests, and (3) a new species of socially parasitic thrips living inside their nests.
In the 12-month Incoming phase, I aimed to test similar hypotheses in a species of sweat bee, Halictus rubicundus – also socially plastic, but in a different way – offspring decide whether to breed alone or help their mother reproduce. By comparing H. rubicundus with D. aneurae, I aimed to provide insights into the role of nutrition for different modes of social behaviour. H. rubicundus is Holarctic and is native to the UK. In this species, in mid-April to mid-May, a mated female digs a nest hole in soil and provisions several cells underground with pollen balls, laying a single egg on each ball. These offspring constitute the first brood (B1), each feeding on the pollen ball as their sole resource, and emerging as adults in June-July. After emergence, the B1 female offspring from northern populations are non-social: they return to their natal nests after a period of foraging - then hibernate over winter, founding new nests the following spring. In southern populations, however, the B1 offspring make a choice: either (1) hibernate and found a nest next spring, i.e. become reproductive, or (2) forgo reproduction and help as a nonreproductive worker at the natal nest, helping the mother produce a second brood of reproductive offspring (B2) who will overwinter and found nests next spring. According to my hypothesis, then, southern offspring receiving poor (i.e. imbalanced) nutrition should decide to be nonreproductive workers, whilst offspring receiving well-balanced nutrition should decide to take the risk of founding their own nest. Northern offspring, by contrast, are all destined to reproduce and should therefore be fed uniformly well-balanced nutrition.
I aimed to ask the following two questions:
1. What is a preferred diet for H. rubicundus? Do larvae raised on experimentally imbalanced diets tend to become workers more readily as adults?
2. Is cooperation in the field correlated with the nutritional value of pollen provided to developing larvae by adults?
After 12 months I have worked towards answering both questions: I am much closer to achieving a workable method with which to answer the first, and data pertaining to the second are still under analysis. However, at this stage neither question can be answered conclusively for the following reasons:
1. Despite using ample numbers of bees for the experiment, not enough bees eventually bred to be statistically analysable. I think this is because of the timing of the seasons: the experiment required transferring bees from Belfast, in the north, to Sussex, in the south, at a critical period when they are about to breed. In 2014 the seasons were mismatched; the Belfast season was unusually late, and bees emerged late; but the Sussex season was unusually early, giving little time for them to breed once transferred.
2. Because of (1), I had to address Objective 2 in a different way; instead of using experimental bees, I instead collected pollen from wild, foraging bees in spring and summer, and in the north and south of the UK. Although successful, more data are required to test the hypothesis.
To address the shortfall in meeting my objectives, I have obtained funding for further collections and experiments to take place outside the timeframe of the Fellowship. I have also obtained a permanent University position which will set the stage for me to obtain grant funding for further experiments.
In the 24-month Outgoing phase, I aimed to test this hypothesis in a socially plastic species of thrips, Dunatothrips aneurae, endemic to the Australian Outback. D. aneurae build silken nests on a variety of Acacia tree in the arid interior of Australia, and some nests are cofounded – i.e. individuals decide to found nests individually or as groups. My objective questions were:
1. What is a “preferred diet” for Dunatothrips aneurae? Do nymphs raised on experimentally imbalanced diets tend to cooperate more readily as adults?
2. Is cooperation in the field correlated with the nutritional value of the plant?
3. Does manipulating the plant’s composition via fertilization affect cooperation in the insect?
4. Does nutritional imbalance affect the division of reproduction within a shared thrips nest?
I am in a position to answer at least one question, with another pending analysis. Two questions proved to be unfeasible to answer within the timeframe of the fellowship in the form I originally proposed. First, I have been able successfully to answer question (2) in the negative: there were no correlations between the nutritional content of the plant and cooperative behaviour in the thrips inhabiting the plant. Thus, using these correlational data I have been able to reject the nutritional constraints hypothesis for D. aneurae.
The complementary question (1), in which I planned to manipulate nutrition for nymphs using artificial diets, has been tricky to answer because of difficulties culturing nymphs in the laboratory. However, I have recently shown that these difficulties were largely due to the thrips’ requirements for high humidity – I have now published a paper demonstrating that the thrips’ nests function to reduce desiccation in the arid outback (Gilbert 2014). With this information, I am now able to plan further lab experiments at controlled, high humidity, but this will be outside the time frame of the fellowship and is a question for future research. I have, however, made progress towards answering this question by conducting a preliminary experiment to ask what a balanced artificial diet looks like for an adult Dunatothrips – I am still analysing the results. Question (3) proved similarly difficult to address, because my pilot studies showed convincingly that the nutritional composition of the Acacia trees do not respond at all to watering or fertilization! This is probably because they are extremely slow-growing and desert-adapted, and possibly also because they have a symbiotic relationship with nutrient-fixing microbes that may provide a buffer against environmental changes such as my manipulations.
To answer question (4) I am analyzing genetic relatedness from over 500 thrips and their offspring from more than 100 nests, having first established suitable microsatellites. This will provide a picture of the genetic structure on trees with different nutritional composition – and whether reproduction on nutrient-poor trees shows the predicted skew in favour of one female.
Since I was able to reject (tentatively) a nutritional explanation for cooperation in Dunatothrips, I conducted behavioural experiments and observations to investigate alternative bases for cooperation in this species. I have published a paper detailing the natural history of D. aneurae, which was previously poorly understood (Gilbert & Simpson 2013) as well as the biology of a new species of social parasite which I found living within their nests (Gilbert et al 2012). I have shown that D. aneurae are pacifists with no defence behaviour, so cooperation is not related to defence. Cooperation may partly be a response to local crowding on branches, as crowded nests are more cooperative. Accordingly, cooperation carries a cost because of competition for space in nests - some females in smaller nests are nonreproductive. These nonreproductive females tend not to help rebuild damaged nests, maybe because they have no genetic stake in offspring.
In summary, my results from the Outgoing phase have provided a rejection of a longstanding hypothesis about social evolution, at least in one species of socially plastic thrips – a valuable contribution to social biology. In addition, I have substantially helped understand D. aneurae biology by publishing (1) an account of its natural history, (2) the exciting discovery of humidity-controlled nests, and (3) a new species of socially parasitic thrips living inside their nests.
In the 12-month Incoming phase, I aimed to test similar hypotheses in a species of sweat bee, Halictus rubicundus – also socially plastic, but in a different way – offspring decide whether to breed alone or help their mother reproduce. By comparing H. rubicundus with D. aneurae, I aimed to provide insights into the role of nutrition for different modes of social behaviour. H. rubicundus is Holarctic and is native to the UK. In this species, in mid-April to mid-May, a mated female digs a nest hole in soil and provisions several cells underground with pollen balls, laying a single egg on each ball. These offspring constitute the first brood (B1), each feeding on the pollen ball as their sole resource, and emerging as adults in June-July. After emergence, the B1 female offspring from northern populations are non-social: they return to their natal nests after a period of foraging - then hibernate over winter, founding new nests the following spring. In southern populations, however, the B1 offspring make a choice: either (1) hibernate and found a nest next spring, i.e. become reproductive, or (2) forgo reproduction and help as a nonreproductive worker at the natal nest, helping the mother produce a second brood of reproductive offspring (B2) who will overwinter and found nests next spring. According to my hypothesis, then, southern offspring receiving poor (i.e. imbalanced) nutrition should decide to be nonreproductive workers, whilst offspring receiving well-balanced nutrition should decide to take the risk of founding their own nest. Northern offspring, by contrast, are all destined to reproduce and should therefore be fed uniformly well-balanced nutrition.
I aimed to ask the following two questions:
1. What is a preferred diet for H. rubicundus? Do larvae raised on experimentally imbalanced diets tend to become workers more readily as adults?
2. Is cooperation in the field correlated with the nutritional value of pollen provided to developing larvae by adults?
After 12 months I have worked towards answering both questions: I am much closer to achieving a workable method with which to answer the first, and data pertaining to the second are still under analysis. However, at this stage neither question can be answered conclusively for the following reasons:
1. Despite using ample numbers of bees for the experiment, not enough bees eventually bred to be statistically analysable. I think this is because of the timing of the seasons: the experiment required transferring bees from Belfast, in the north, to Sussex, in the south, at a critical period when they are about to breed. In 2014 the seasons were mismatched; the Belfast season was unusually late, and bees emerged late; but the Sussex season was unusually early, giving little time for them to breed once transferred.
2. Because of (1), I had to address Objective 2 in a different way; instead of using experimental bees, I instead collected pollen from wild, foraging bees in spring and summer, and in the north and south of the UK. Although successful, more data are required to test the hypothesis.
To address the shortfall in meeting my objectives, I have obtained funding for further collections and experiments to take place outside the timeframe of the Fellowship. I have also obtained a permanent University position which will set the stage for me to obtain grant funding for further experiments.