Leticia Avilés

Interdemic Selection and the Sex Ratio: A Social Spider Perspective

Computer simulations of a metapopulation model that mimics social spider populations show that highly female-biased sex ratios evolve when continuously inbreeding lineages (colonies) proliferate differentially to replace other lineages that have become extinct. When lineages of any size proliferated, that is, when the advantage to the colony of producing more females was removed, biased sex ratios did not evolve despite extreme conditions of inbreeding. Selection at the colony level is therefore necessary to counteract Fisherian selection within colonies, which here is shown to be acting regardless of the degree of population subdivision. Smaller size of the founding groups and lower migration rates resulted in more female-biased sex ratios because they reduced the within-group genetic variance and increased the variance among groups and therefore made selection among groups more effective. The outcome of the selective process, however, depended not only on the degree of population subdivision (i.e., the ratio of the variances), but also on the relative rate of turnover of the groups and the individuals within them: the lower the rate of colony turnover, the less biased the equilibrium sex ratio. The threshold size for proliferation, brood size, and conditional control over the production of at least one male also affected the equilibrium sex ratio under some of the conditions investigated

Sex-Ratio Bias and Possible Group Selection in the Social Spider Anelosimus eximius

A demographic study on the social spider Anelosimus eximius (Araneae: Theridiidae) demonstrates no differential mortality of the sexes during the age of reproduction and no large difference in their maturation times to explain the highly female-biased sex ratios in adults. Moreover, sex ratios within the range of 0.04 to 0.40 males per female are already present at the earliest stage at which sexes can be distinguished in the field. Fishers theory predicts a 1:1 sex ratio as evolutionarily stable. How, then, are the observed ratios attained and maintained? It is suggested that the unique population structure and dynamics of this social spider resulted in a change of balance between the opposing forces of group and individual selection, making evolutionarily stable a sex ratio that increases colony survival and proliferation.

Colony Size and Individual Fitness in the Social Spider Anelosimus eximius

The effects of colony size on individual fitness and its components were investigated in artificially established and natural colonies of the social spider Anelosimus eximius (Araneae: Theridiidae). In the tropical rain forest understory at a site in eastern Ecuador, females in colonies containing between 23–107 females had india significantly higher lifetime reproductive success than females in smaller colonies. Among larger colonies, this trend apparently reversed. This overall fitness function was a result of the conflicting effects of colony size on different components of fitness. In particular, the probability of offspring survival to maturity increased with colony size while the probability of a female reproducing within the colonies decreased with colony size. Average clutch size increased with colony size when few or no wasp parasitoids were present in the egg sacs. With a high incidence of egg sac parasitoids, this effect disappeared because larger colonies were more likely to be infected. The product of the three fitness components measured—probability of female reproduction, average clutch size, and offspring survival—produced a function that is consistent with direct estimates of the average female lifetime reproductive success obtained by dividing the total number of offspring maturing in a colony by the number of females in the parental generation. Selection, therefore, should favor group living and itermediate colony sizes in this social spider.

SOCIALITY IN THERIDIID SPIDERS: REPEATED ORIGINS OF AN EVOLUTIONARY DEAD END

Abstract Evolutionary “dead ends” result from traits that are selectively advantageous in the short term but ultimately result in lowered diversification rates of lineages. In spiders, 23 species scattered across eight families share a social system in which individuals live in colonies and cooperate in nest maintenance, prey capture, and brood care. Most of these species are inbred and have highly female-biased sex ratios. Here we show that in Theridiidae this social system originated eight to nine times independently among 11 to 12 species for a remarkable 18 to 19 origins across spiders. In Theridiidae, the origins cluster significantly in one clade marked by a possible preadaptation: extended maternal care. In most derivations, sociality is limited to isolated species: social species are sister to social species only thrice. To examine whether sociality in spiders represents an evolutionary dead end, we develop a test that compares the observed phylogenetic isolation of social species to the simulated evolution of social and non-social clades under equal diversification rates, and find that sociality in Theridiidae is significantly isolated. Because social clades are not in general smaller than their nonsocial sister clades, the “spindly” phylogenetic pattern—many tiny replicate social clades—may be explained by extinction rapid enough that a nonsocial sister group does not have time to diversify while the social lineage remains extant. In this case, this repeated origin and extinction of sociality suggests a conflict between the short-term benefits and long-term costs of inbred sociality. Although benefits of group living may initially outweigh costs of inbreeding (hence the replicate origins), in the long run the subdivision of the populations in relatively small and highly inbred colony lineages may result in higher extinction, thus an evolutionary dead end.

Cooperative capture of large prey solves scaling challenge faced by spider societies

A decrease in the surface area per unit volume is a well known constraint setting limits to the size of organisms at both the cellular and whole-organismal levels. Similar constraints may apply to social groups as they grow in size. The communal three-dimensional webs that social spiders build function ecologically as single units that intercept prey through their surface and should thus be subject to this constraint. Accordingly, we show that web prey capture area per spider, and thus number of insects captured per capita, decreases with colony size in a neotropical social spider. Prey biomass intake per capita, however, peaks at intermediate colony sizes because the spiders forage cooperatively and larger colonies capture increasingly large insects. A peaked prey biomass intake function would explain not only why these spiders live in groups and cooperate but also why they disperse only at large colony sizes, thus addressing both sociality and colony size range in this social spider. These findings may also explain the conspicuous absence of social spiders from higher latitudes and higher elevations, areas that we have previously shown to harbor considerably fewer insects of the largest size classes than the lowland tropical rainforests where social spiders thrive. Our findings thus illustrate the relevance of scaling laws to the size and functioning of levels of organization above the individual.

Survival benefits select for group living in a social spider despite reproductive costs

The evolution of cooperation requires benefits of group living to exceed costs. Hence, some components of fitness are expected to increase with increasing group size, whereas others may decrease because of competition among group members. The social spiders provide an excellent system to investigate the costs and benefits of group living: they occur in groups of various sizes and individuals are relatively short‐lived, therefore life history traits and Lifetime Reproductive Success (LRS) can be estimated as a function of group size. Sociality in spiders has originated repeatedly in phylogenetically distant families and appears to be accompanied by a transition to a system of continuous intra‐colony mating and extreme inbreeding. The benefits of group living in such systems should therefore be substantial. We investigated the effect of group size on fitness components of reproduction and survival in the social spider Stegodyphus dumicola in two populations in Namibia. In both populations, the major benefit of group living was improved survival of colonies and late‐instar juveniles with increasing colony size. By contrast, female fecundity, female body size and early juvenile survival decreased with increasing group size. Mean individual fitness, estimated as LRS and calculated from five components of reproduction and survival, was maximized for intermediate‐ to large‐sized colonies. Group living in these spiders thus entails a net reproductive cost, presumably because of an increase in intra‐colony competition with group size. This cost is traded off against survival benefits at the colony level, which appear to be the major factor favouring group living. In the field, many colonies occur at smaller size than expected from the fitness curve, suggesting ecological or life history constraints on colony persistence which results in a transient population of relatively small colonies.

Solving the freeloaders paradox: Genetic associations and frequency-dependent selection in the evolution of cooperation among nonrelatives

One of the enduring problems in the study of social evolution has been to understand how cooperation can be maintained in the presence of freeloaders, individuals that take advantage of the more cooperative members of groups they are eager to join. The freeloader problem has been particularly troublesome when groups consist of nonrelatives, and no inclusive fitness benefits accrue to individuals that contribute more heavily to communal activities. These theoretical difficulties, however, are not mirrored by the numerous examples of cooperative or even altruistic behaviors exhibited by groups of nonrelatives in nature (e.g., many human groups, communally nesting bees, multiple queen-founding ants, cellular slime molds, and social bacteria). Using a model in which cooperation and grouping tendencies are modeled as coevolving dynamical variables, I show that the freeloader problem can be addressed when group-size effects on fitness are considered explicitly. I show that freeloaders, whose presence is reflected in the development of linkage disequilibrium between grouping and cooperation, increase in frequency when rare, but are selected against when common due to the reduced productivity of the groups they overburden with their presence. Freeloader frequencies thus periodically rise and fall around an equilibrium shown here to be dynamic. These results highlight the importance of group-level effects in the origin and maintenance of sociality, illustrate the dynamic nature of equilibria when multiple levels of selection are involved, and provide a solution to the freeloaders paradox.

Population differences in behaviour are explained by shared within-population trait correlations

Correlations in behavioural traits across time, situation and ecological context (i.e. ‘behavioural syndromes’ or ‘personality’) have been documented for a variety of behaviours, and in diverse taxa. Perhaps the most controversial inference from the behavioural syndromes literature is that correlated behaviour may act as an evolutionary constraint and evolutionary change in one’s behaviour may necessarily involve shifts in others. We test the two predictions of this hypothesis using comparative data from eighteen populations of the socially polymorphic spider, Anelosimus studiosus (Araneae, Theriidae). First, we ask whether geographically distant populations share a common syndrome. Second, we test whether population differences in behaviour are correlated similarly to within‐population trait correlations. Our results reveal that populations separated by as much as 36° latitude shared similar syndromes. Furthermore, population differences in behaviour were correlated in the same manner as within‐population trait correlations. That is, population divergence tended to be along the same axes as within‐population covariance. Together, these results suggest a lack of evolutionary independence in the syndrome’s constituent traits.

Altitudinal Patterns of Spider Sociality and the Biology of a New Midelevation Social Anelosimus Species in Ecuador

To the extent that geography correlates with particular environmental parameters, the geographical distribution of phylogenetically related social and nonsocial organisms should shed light on the conditions that lead to sociality versus nonsociality. Social spiders are notorious for being concentrated in tropical regions of the world, occupying a set of habitats more restricted than those available to the phylogenetic lineages in which they occur. Here we document a parallel pattern involving elevation in the spider genus Anelosimus in America and describe the biology of a newly discovered social species found at what appears to be the altitudinal edge of sociality in the genus. We show that this is a cooperative permanent‐social species with highly female‐biased sex ratios but colonies that are one to two orders of magnitude smaller than those of a low‐elevation congener of similar body size. We suggest that the absence of subsocial Anelosimus species in the lowland rain forest may be due to an increased probability of maternal death in this habitat due to greater predation and/or precipitation, while absence of a sufficient supply of large insects at high elevations or latitudes may restrict social species to low‐ to midelevation tropical moist forests. We refer to these as the “maternal survival” and “prey size” hypotheses, respectively, and suggest that both in combination may explain the geographical distribution of sociality in the genus.

Natal dispersal and demography of a subsocial Anelosimus species and its implications for the evolution of sociality in spiders

The transition to permanent-sociality in spiders is thought to have involved the suppression of the dispersal phase characteristic of hypothetical subsocial or periodic-social ancestral species. Extant periodic-social species may provide insights into this transition. The periodic-social Anelosimus jucundus in southern Arizona was found to form mother-offspring and sibling associations that disintegrate prior to the mating season. Following the breakdown of the social phase, more than twice as many females as males became established within a few metres of the natal nest. Given that the predispersal sex ratio was 1:1, a fraction of the males may have dispersed beyond the local area. The short dispersal distances of at least a fraction of individuals of both sexes, the clustering of nests in local areas, and at least two possible cases of sibling mating suggest, however, that dispersal may not eliminate the possibility of close inbreeding in this species. Estimated transition probabilities between life-history stages show that the heaviest loss of individuals occurs during dispersal. Once established, 41% of the females that reached maturity succeeded in producing grown progeny. We discuss the implications of these findings in terms of the transition from periodic to permanent sociality in spiders and of current models that consider the interplay between competition and inbreeding avoidance in the evolution of dispersal.