Cooperation is said to occur when the behavior of one individual benefits others (West et al., 2021). This tends to lead to grouping as individuals stick together in order to accrue benefits from the actions of their neighbors. The essence of sociality has been described as “reciprocal communication of a cooperative nature” (Wilson, 1971), since, by definition, an individual can only incur benefits from remaining in a group if others remain there as well.

Kin selection has historically been considered the driving force in insect sociality, whereby individuals reap indirect fitness benefits by helping closely related kin. However, recent work has challenged this paradigm (Nowak et al., 2010), suggesting that direct fitness benefits can drive cooperation in insect groups, even among classically eusocial Hymenoptera (Hölldobler and Wilson, 2008; Leadbeater et al., 2011; Brahma et al., 2019). Direct benefits from natural selection that don’t require kinship between cooperators are thus receiving increasing attention as an alternative framework for understanding insect sociality (Leimar and Hammerstein, 2010; West et al., 2021).

The broad diversity of social forms across multiple insect species provides valuable insights into the evolution and ecology of sociality beyond the hymenopteran eusocial continuum (Choe and Crespi, 1997; Costa, 2006; Rubenstein and Abbot, 2017); these have evolved independently and are likely driven by different selection pressures. This paper examines one phylogenetically widespread “alternative” form of insect sociality, herding of herbivorous insect larvae. This describes larval insects that aggregate and use a variety of mechanisms to remain together on their host plant, often gradually dispersing as they grow larger and becoming solitary as adults. Larval herds lack parent-offspring interaction and often include unrelated individuals (Costa, 2018) and thus challenge us to think beyond the eusocial model when considering insect sociality. They can provide unique insights into ecological drivers of sociality.

Herds often arise from the same egg mass and thus can be made up of siblings, suggesting the possibility for indirect benefits via kin selection. Indeed, cooperation is considered more likely to occur when population structure favors grouping of related individuals, due to indirect benefits that accrue from cooperating with relatives (Wilson, 1971). However, cooperation can be favored by natural selection if it is mutually beneficial and directly benefits the actor as well as recipients, whether they are related or not. Cooperation only appears paradoxical if it incurs a cost to the cooperator, which is not always the case (Leadbeater et al., 2011; Brahma et al., 2019). Indeed, recent work shows strong evidence for substantial direct benefits of cooperation in multiple animal taxa (West et al., 2021). Thus, although kin selection could play a role in favoring cooperation in larval herds, it is not necessarily required and direct benefits could provide more parsimonious explanations (Nowak et al., 2010). Existing evidence suggests that kin selection is not essential to promote herding: group mixing occurs in the few species in which the genetic structure of herds has been investigated, and no species studied to-date show any evidence of kin recognition (Costa, 2018).

This paper examines benefits of grouping in larval herds taking a direct fitness perspective, i.e., examining advantages to the individual of staying in the group vs. leaving. This approach remains neutral as to whether kin selection is involved, and focuses instead on the natural selection drivers of social behaviors. These occur independently of any putative indirect benefits. Evidence suggests that individual larvae weigh costs and benefits of remaining with the group and do leave herds when remaining becomes costly (Plenzich and Despland, 2018). Larval herding thus appears to be an instance where cooperation is mutually beneficial and hence where direct fitness benefits play an important role.

Larval gregariousness is observed in many insect species across several orders (Costa, 2006). The best studied species are Lepidopteran caterpillars, but examples are also known among sawfly (Hymenoptera) and beetle (Coleoptera) larvae and grasshopper (Orthoptera) nymphs. Many of these species clearly actively aggregate, rather than merely staying together following hatching on a high quality food source. There is no evidence for kin recognition in those species where it has been studied [caterpillars (Costa and Louque, 2001; Costa and Ross, 2003; Sun and Underwood, 2011) and sawflies (Terbot et al., 2017)]. Division of labor has been suggested in some species (Ghent, 1960; Underwood and Shapiro, 1999), but was not detected in others (Costa and Ross, 2003; McClure et al., 2011b) and does not seem to play a major role.

The mechanisms used by individuals to remain with the group have been studied in detail in several species, showing a range of sophisticated forms of communication whose main purpose appears to be keeping the group together (Despland, 2013). The best-known is pheromone trail following (see https://alisonloader.com/mass-transit/ for an artist’s manipulation of trail-following caterpillars by drawing artificial pheromone trails). This mechanism has been documented in caterpillars (Peterson, 1988; Roessingh, 1989; Fitzgerald, 1993b,a; Fitzgerald and Underwood, 1998; Ruf et al., 2001; Costa and Gotzek, 2003; Fitzgerald and Pescador-Rubio, 2011; Pescador-Rubio et al., 2011), beetle (Fitzgerald et al., 2004) and sawfly larvae (Costa and Louque, 2001). Other mechanism to maintain group cohesion include allomimesis (Despland et al., 2017) and processions (Fitzgerald, 2003) in caterpillars, and synchronization of movement (Despland and Simpson, 2006; Despland, 2020) in grasshopper nymphs. The existence of these behaviors underscores the benefits of cooperation, since they have clearly been shaped by natural selection to ensure that individuals do not get separated from the group (Hofmann et al., 2014).

Herding larvae exhibit various forms of social organization, generally categorized by different modes of foraging. Some larvae exhibit patch restricted foraging whereby the herd forms a shelter, often by spinning silk, and feed on the foliage enclosed within the shelter. Others are nomadic, using pheromone trails or other cues to move together between feeding sites. Some of the best studied species are central place foragers that build a shelter (again often using silk) then move out of the shelter to find food sources (Costa and Pierce, 1997; Fitzgerald and Costa, 1999). Broadening phylogenetic and geographic scope has shown myriad variations on these themes, including species that change between different organizational structures during larval development (Costa, 2006).

Most larval herds begin as sib-groups that emerge from the same egg mass, but fail to disperse. There are many reasons why herbivorous female insects might lay eggs in clusters on host plants, including constraints on the adult female (e.g., difficulty in host finding, short longevity), benefits to the eggs (e.g., protection from freezing or desiccation) and grouping of larval progeny once they emerge from the egg (Stamp, 1980). However, in many species that lay eggs in clusters, the larvae disperse upon hatching, suggesting that larval gregariousness can be selected for separately from egg-clustering.

At high population densities, larvae from different egg masses can fuse into large herds of multiple sib-groups (Costa and Ross, 2003; Fletcher, 2009). Indeed, some species preferentially lay eggs close to conspecific egg-masses (see Figure 1), presumably in order to increase group size (Stamp, 1980; Codella and Raffa, 1993). In the single species studied, this was shown to be adaptive due to the increase in group size despite the dilution of relatedness (Costa and Ross, 2003). Groups are often most cohesive early in caterpillar ontogeny, and caterpillars often disperse in the later instars, suggesting that benefits of grouping decrease as caterpillars grow larger (Despland and Hamzeh, 2004; Colasurdo and Despland, 2005; Despland and Huu, 2007). Herds can also dissolve under poor food conditions, as larvae move away to forage individually (Plenzich and Despland, 2018). The cost-benefit ratio of cooperation thus varies over larval ontogeny and in different environments (Guindre-Parker and Rubenstein, 2020).

Several different advantages to larval herding have been proposed in various insect species, and these can be grouped into broad categories based on the driving selection pressure: environmental pressures, bottom up forces from host plants, and top-down forces from natural enemies. I review these in the following sections and discuss contexts in which they might apply.

Insect larvae are poikilothermic and therefore suffer slower metabolism, growth and development at lower temperature. Several caterpillar species have been shown to reap thermal gains from collective basking (Table 1 and Figure 2) under conditions of relatively low temperature but high solar radiation. This cooperative thermoregulation sometimes includes the construction of a shelter or tent that can be used to further increase caterpillar body temperature (Table 1).

Larval grouping has also been suggested to facilitate physiological regulation by preventing water loss. Improved water balance has been shown in aggregations of Imbrasia belina (Westwood) (Saturniidae) caterpillars in South Africa (Klok and Chown, 1999) and Chlosyne lacinia (Geyer) (Nymphalidae) in Arizona (Clark and Faeth, 1997), as well as within the tents of Inachis io (Linnaeus, 1758) (Nymphalidae) in the United Kingdom (Willmer, 1980). However, no discernable effect of aggregation was shown on water loss in Eutrichia capensis (Lasiocampidae) in South Africa (Schoombie et al., 2013). It has been noted that insects feeding on foliage (which always has a high water content) are not likely to face great risk of desiccation except during periods of food deprivation (Klok and Chown, 1999).

Further investigation of species that show thermal gains in aggregations have shown that caterpillars can modulate their grouping behavior depending on ambient conditions. Caterpillars move to a basking spot under a heat lamp at low temperatures but not at high ones, and aggregation is tightest under conditions where it is most beneficial (low temperature and high solar radiation) (McClure et al., 2011a). Tent-builders move around inside the tent during the day to optimize temperature (Joos et al., 1988; Ruf and Fiedler, 2002; Ruf et al., 2003).

Many of the species that bask collectively to elevate body temperature are early spring feeders of the temperate zone (Table 1). These caterpillars hatch in early spring to feed on expanding foliage, which is generally softer and more nutritious than mature foliage (Despland, 2018) and to use the enemy-free space before many predators become active (Parry et al., 1998). However, these caterpillars emerge when temperatures are below optimal for growth and development, even below freezing (Despland, 2021), and many show adaptations that increase thermal gains from radiant solar energy: dark color, dense setae (Casey and Hegel, 1981), and collective basking.

A few notable well-documented biogeographical outliers include species that are active during winter in cool regions (Thaumatopoea pityocampa (Notodontidae) in the Mediterranean and Eucheira socialis (Pieridae) in Mexico) and cooperate to build tents to maximize solar radiation (Fitzgerald and Underwood, 2000; Uemura et al., 2020). As in the early-spring feeders above, these caterpillars are active at low, even below-freezing, temperatures, when cooperative thermoregulation is most advantageous.

Thermoregulation thus seems to have played an important role in shaping the biology of cold-weather active caterpillars, including their cooperative basking and shelter-building behavior (Joos et al., 1988; Joos, 1992; Despland, 2013). The best-studied among these are early-spring feeders in temperate-zone-inhabiting members of the Lasiocampidae. Collective thermoregulatory behaviors are often associated with other traits like dark pigmentation and dense setae that also improve heat capture; cooperative thermoregulation is thus part of an adaptive suite of traits associated with the niche of early spring feeding that is particularly common among the Lasiocampidae. There are close to 2,000 species in the family; it is not known how many of these have gregarious larvae, nor are the phylogenetic relationships between them clear (Regier et al., 2000; Zolotuhin et al., 2012). It has been suggested that gregarious larvae have evolved three separate times within the Lasiocampidae (Regier et al., 2000), but clearly much remains to be understood about the evolution of larval cooperation in this family and the role played by cooperative thermoregulation.

Among the evolutionary drivers underlying larval herding behavior, collective thermoregulation is reasonably well-established. However, although pressures from host plants and predators/parasitoids are often cited as important, they have received less critical analysis. In particular, further work on escaping induced plant defenses and on the relationship between grouping and warning signals could open up important new perspectives in the fields of plant-insect interactions and aposematic theory respectively.

It remains far from clear how collective feeding would allow larval insects to overcome or circumvent plant chemical defenses (see Table 2). One suggested mechanism is that insects feeding in synchrony maximize food intake before induced defenses become expressed (Anderson et al., 2015). The study of plant metabolic pathways underlying induced defense is a field that is progressing rapidly, which provides opportunities for investigating benefits to collective feeding at the molecular level [for example de Bobadilla et al. (2021)]. Improved understanding of these advantages could generate meaningful insights into the temporal and spatial feeding patterns of herbivores in general.

Similarly, many questions remain about how aposematism first evolved and how the costs and benefits of warning coloration depend on context (Ruxton et al., 2019). It is increasingly apparent that the adaptive value of color defenses must be understood in the context of suites of functionally related traits that tend to co-vary (Caro and Ruxton, 2019). Indeed, an organism’s overall phenotype combines multiple traits and is a response to multiple selection pressures (Pigliucci, 2003). For instance, feeding on toxic plants, gregarious behavior and warning coloration are traits that are frequently expressed together, and that can also be associated with sluggishness, slow growth rate and conspicuous positioning (Despland, 2020). Physiological and biochemical traits related to detoxification, transformation and/or sequestration of plant compounds are likely also associated. Phenotypic integration (Pigliucci, 2003) implies that the adaptive value of each of these traits must be explored in the context of variation in the other functionally related traits. Investigating interactions between these traits and how they are shaped by both bottom-up and top-down selection pressures could provide novel insights to the field of aposematic theory. More generally, applying the phenotypic integration approach to studying the different suites of traits that include larval herding (e.g., the thermoregulating early-spring feeders, the aposematic toxic-plant eaters, etc.) could provide a useful framework to make sense of the complex diversity of social behaviors of herbivorous insect larvae.

In conclusion, this paper shows abundant evidence for direct benefits to larval herding, suggesting that kin selection is not required to explain why hatching insect siblings aggregate. It is worth mentioning that this does not shed any light on the question of whether kin selection occurs as well, since kin selection and natural selection can operate as independent processes (West et al., 2021). Theoretical models of the evolution of insect sociality also examine the potential roles of various levels of selection, raising the possibility that selection could operate on the whole group as well as on the individual (Traulsen and Nowak, 2006; Hölldobler and Wilson, 2008). Indeed, interactions between group members can generate emergent group-level traits that influence individual survival (Wellington, 1960; Myers, 2000): for instance in E. lanestris, maintenance of an intact tent is the best predictor of survival of at least one individual of a group (Ruf and Fiedler, 2005). Larval herds thus provide a model system amenable to examining group-level selection, one that is perhaps particularly tractable due to its simple demographic structure.

Finally, it must be noted that only a small minority of herding larvae have been studied and therefore it would be premature to generalize about selective drivers of this alternative yet surprisingly widespread form of insect sociality. Tropical species in particular exhibit a wide range of striking collective behaviors that remain uninvestigated, and for which we can at present only speculate as to their function: for example, rolling swarm caterpillars¹ or wriggling bunches of sawfly larvae². The temperate zone bias (Zuk, 2016) applies to the study of cooperative behavior in insect larvae as well as to other areas of ecology, and implies that there remains much to be discovered.

ED wrote the manuscript.

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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