James T. Costa

Fitness effects of group merging in a social insect

Animal social groups often consist of non–relatives, a condition that arises in many cases because of group merging. Although indirect fitness contributions are reduced in such groups compared with those in groups composed of close kin, the genetic–heterogeneity hypothesis suggests that these groups may benefit from increased intracolony genetic variation, which may boost group performance through increased task efficiency or parasite resistance. We confirm one prediction of the task–efficiency explanation by demonstrating a genetic basis for task thresholds of socially important behaviours in eastern tent caterpillars. However, we found no evidence that the expanded range of task thresholds in mixed colonies translates into improved individual or colony performance in the field. By contrast, increased group size, a less commonly considered correlate of group mixing, was found to enhance individual fitness through its effects on larval growth. We conclude that fitness benefits offsetting the dilution of relatedness in heterogeneous social groups may often stem from augmented group size rather than increased genotypic diversity.

Collective behavior in social caterpillars

The repertoires of social caterpillars are drawn from four categories of behavior centered on shelter building, thermoregulation, colony defense, and trail-based communication. This chapter provides an overview of these collective patterns of behavior and assesses the potential role of individual-level behavior in their overt expression. While few of the 300 or more species of caterpillars that form sib-aggregations have been studied in any detail, our review of the literature indicates that the most promising fronts for the investigation of emergent phenomena in social caterpillars lie in the areas of collective shelter building and trail-marking behavior. Of particular interest is the resemblance of trail-based chemical recruitment communication and collective flexibility in recruitment in caterpillars to similar phenomena in the Hymenoptera. The decision rules underlying recruitment patterns have been explored in ants, and are likely to prove generalizable to the more sophisticated of the recruitment systems found among the lasiocampid caterpillars, but a set of mechanisms dependent on such species-specific factors as resource patchiness, mode of recruitment, and physical properties of silk are likely to uniquely influence collective foraging patterns and shelter-building behavior in social caterpillars.

Trail-Based Communication in Social Caterpillars of Eriogaster lanestris (Lepidoptera: Lasiocampidae)

Caterpillars of Eriogaster lanestris (Lepidoptera: Lasiocampidae) mark trails as they move between feeding sites and their communal tent. They prefer new trails over aged ones. Hungry caterpillars prefer trails marked by fed caterpillars returning to the tent. Thus successful foragers direct tentmates to profitable food finds, in a manner similar to that of Malacosoma americanum. E. lanestris readily follows trails prepared from 5β-cholestane-3-one, a component of the trail marker of M. americanum, when applied at a rate of ≥10−10 g/cm. In choice tests, they preferred more highly concentrated over weaker trails. New trails are always established in groups, and the velocity increases from early to late caterpillars traversing a new trail.

HIERARCHICAL GENETIC STRUCTURE AND GENE FLOW IN MACROGEOGRAPHIC POPULATIONS OF THE EASTERN TENT CATERPILLAR (MALACOSOMA AMERICANUM

Genetic structure and inferred rates of gene flow in macrogeographic populations of the eastern tent caterpillar Malacosoma americanum were analyzed at two hierarchical scales: local demes and regional subpopulations. Wrights F‐statistics were used to estimate population genetic structure using multilocus genotypic data generated electrophoretically. Estimated values of FST and the distribution of private alleles were then used to obtain indirect estimates of gene flow. We found modest, though significant, genetic structure at both spatial scales, a pattern consistent with high rates of gene flow over the large distances involved. Modest values obtained for Neis genetic distance also suggested high levels of gene flow across the range of this species, although some gene‐flow restriction resulting from isolation by distance was suggested by a positive regression of genetic distance on geographic distance. The observed homogeneity at enzyme loci across the range of M. americanum parallels the reported uniformity in morphology, suggesting a general absence of local genetic differentiation in this widely distributed species. The genetic homogeneity observed in this wide‐ranging insect is discussed in terms of organism‐specific environmental experience at different spatial scales. Some organisms occupying apparently heterogeneous environments may ameliorate unsuitable local conditions through microhabitat selection or behavioral modification of their microenvironment. This may be accomplished in M. americanum through group shelter construction and behavioral thermoregulation, closely tying thermoregulation to social biology in this species. If in this way the tent helps produce an effectively homogeneous environment for this species across its extensive range, this system may provide a unique example of how social behavior can influence the distribution of genetic variation in a population.

Group Foraging and Trail following Behavior of the Red-headed Pine Sawfly Neodiprion lecontei (Fitch) (Hymenoptera: Symphyta: Diprionidae)

Abstract Larval sawfly foraging behavior is understudied in comparison to defoliating Lepidoptera, yet the parallel lifestyles of these groups suggest that similar behavioral and physiological adaptations may have arisen in response to common selective pressures. The red-headed pine sawfly, Neodiprion lecontei (Fitch), is a gregarious diprionid that forages nomadically on a variety of pine species. We investigated the behavioral basis of group foraging in N. lecontei, in particular trail following and colony foraging dynamics, in order to better understand the mechanisms contributing to group cohesion in this species. We show that N. lecontei is, like many social Lepidoptera, a trail follower, showing a strong preference for substrate contacted by foraging conspecifics. This may be the first study to demonstate trail following behavior in a social sawfly. In ad libitum group movement studies, larval groups did not colonize new patches in a single migratory pulse but migrated over a period of hours solitarily or in small groups. Foraging groups remained largely cohesive yet frequently fissioned small groups that dynamically recoalesced during larval development. We speculate that N. lecontei larvae remain cohesive by cueing on a marker derived from their pine host and deposited passively by migrating conspecifics.

The Darwinian Revelation: Tracing the Origin and Evolution of an Idea

The idea of evolution by natural selection formulated by Charles Darwin and Alfred Russel Wallace is a cornerstone of modern biology, yet few biology students or professionals are familiar with the processes of discovery behind the idea. Focusing on Darwin, I draw on letters, notebooks, and other resources to trace key insights and put them into historical context, illustrating how major elements of Darwins theory came to him over many years. I further consider how Darwin came to formulate the logical argument structure of his Origin of Species, discussing the philosophical arguments inherent in the books structure and how this and Darwins other works can be seen as part of a larger argument and way of looking at the world. I suggest that in teaching evolution today, educators could profitably draw on both Darwins personal intellectual journey in coming to his ideas, and the compelling argument structure he devised in presenting his theory.

Trail marking and processionary behavior of the larvae of the weevil Phelypera distigma (Coleoptera: Curculionidae)

We present here the results of an investigation of the behavioral bases of the first documented instance of trail marking and processionary behavior in a beetle. The larvae of Phelypera distigma (Coleoptera: Curculionidae) forage communally, moving over the host plant in head-to-tail processions. Our study shows that the larvae secrete a pheromone from the ventral surface of the posterior abdomen that both elicits and guides the collective locomotion of the cohort. The pheromone is soluble in acetone and other nonpolar solvents and is relatively short-lived, eliciting trail following for less than 4 h after its deposition. When in processionary formations, larvae stimulate locomotion in others by rapidly bobbing their heads against sets of setae that occur on the lateral flanks of the posterior tips of the abdomens of precedent individuals. Larvae are also strongly attracted to tactile or chemotactile stimuli found at the tip of the abdomen of other larvae and their response to lures made of eviscerated abdomens show that such stimuli take precedence over the trail pheromone in eliciting and orienting locomotion. The cycloalexic formations adopted by resting larvae maximize the amount of body contact possible in a two-dimensional aggregate and allow tactile signals to rapidly radiate through the groups, alerting all members of a cohort to the onset of bouts of activity.

Larval Communication and Group Foraging Dynamics in the Red-Headed Pine Sawfly, Neodiprion lecontei (Fitch) (Hymenoptera: Symphyta: Diprionidae)

Abstract The red-headed pine sawfly, Neodiprion lecontei (Fitch), is a gregarious diprionid common in eastern and north-central North America. Larvae of this species have been shown to use trail pheromones to maintain colony structure. Herein we report the results of further studies of group foraging behavior, showing that tactile cues or contact chemoreception also play a role in maintaining colony structure. Video-based activity records reveal a pattern of synchronized, continuous daily feeding punctuated by short periods of quiescence. Y-maze experiments and video examination of group movement revealed that exploring larvae are strongly influenced in the selection of new feeding sites by the presence of conspecifics at those sites. Larvae settled and initiated feeding more quickly at feeding sites at which conspecifics were already present. This was also true when freeze-killed groups of conspecifics were used, suggesting that physical contact and not active signaling plays a role in group cohesion. In the absence of conspecifics, larval site selection is influenced by trail pheromones deposited by earlier-exploring larvae. Our studies suggest red-headed pine sawflies use two-tiered or hierarchical communication cues necessitated by the loose manner in which groups colonize new feeding sites. Trail pheromones may help foraging larvae relocate their colony or its general vicinity, but foragers tend to remain active until they physically contact conspecifics.

Engaging with Lyell: Alfred Russel Wallace's Sarawak Law and Ternate papers as reactions to Charles Lyell's Principles of Geology

Abstract Alfred Russel Wallace (1823–1913) and Charles Darwin (1809–1882) are honored as the founders of modern evolutionary biology. Accordingly, much attention has focused on their relationship, from their independent development of the principle of natural selection to the receipt by Darwin of Wallace’s essay from Ternate in the spring of 1858, and the subsequent reading of the Wallace and Darwin papers at the Linnean Society on 1 July 1858. In the events of 1858 Wallace and Darwin are typically seen as central players, with Darwin’s friends Charles Lyell (1797–1875) and Joseph Dalton Hooker (1817–1911) playing supporting roles. This narrative has resulted in an under-appreciation of a more central role for Charles Lyell as both Wallace’s inspiration and foil. The extensive anti-transmutation arguments in Lyell’s landmark Principles of Geology were taken as the definitive statement on the subject. Wallace, in his quest to solve the mystery of species origins, engaged with Lyell’s arguments in his private field notebooks in a way that is concordant with his engagement with Lyell in the 1855 and 1858 papers. I show that Lyell was the object of Wallace’s Sarawak Law and Ternate papers through a consideration of the circumstances that led Wallace to send his Ternate paper to Darwin, together with an analysis of the material that Wallace drew upon from the Principles. In this view Darwin was, ironically, intended for a supporting role in mediating Wallace’s attempted dialog with Lyell.

Hamiltonian inclusive fitness: a fitter fitness concept

In 1963–1964 W. D. Hamilton introduced the concept of inclusive fitness, the only significant elaboration of Darwinian fitness since the nineteenth century. I discuss the origin of the modern fitness concept, providing context for Hamiltons discovery of inclusive fitness in relation to the puzzle of altruism. While fitness conceptually originates with Darwin, the term itself stems from Spencer and crystallized quantitatively in the early twentieth century. Hamiltonian inclusive fitness, with Prices reformulation, provided the solution to Darwins ‘special difficulty’—the evolution of caste polymorphism and sterility in social insects. Hamilton further explored the roles of inclusive fitness and reciprocation to tackle Darwins other difficulty, the evolution of human altruism. The heuristically powerful inclusive fitness concept ramified over the past 50 years: the number and diversity of ‘offspring ideas’ that it has engendered render it a fitter fitness concept, one that Darwin would have appreciated.