Andrew G. Zink

The Evolution of Intraspecific Brood Parasitism in Birds and Insects.

Many species of birds and insects engage in intraspecific brood parasitism (IBP), when a female lays eggs in the nest of a conspecific and leaves without providing parental care. These visiting females may also act to cooperate with a primary female, staying to provide parental care. Therefore, IBP and cooperative breeding can be considered extremes on a continuum of parental care provided by a secondary female. When a secondary female abandons a nest, she creates an asymmetry in parental care between herself and the host. While models of asymmetry in reproductive allocation have focused directly on relatedness between females, we lack an appropriate theoretical framework that addresses the effects of relatedness on parental care asymmetry. Here, I present an evolutionarily stable strategy (ESS) model that predicts the conditions under which IBP is favored over cooperation and solitary breeding. Intraspecific brood parasitism is less likely to evolve (relative to cooperation and solitary breeding) as the relatedness between a host and parasite increases. It can evolve, however, if parasites achieve a high overall fecundity relative to solitary females. Constraints on solitary breeding can further promote IBP under some circumstances. Cooperation is favored when relatedness is high and reproductive skew is low. This model makes several predictions regarding the conditions under which IBP may evolve, motivating a variety of experimental approaches.

Intraspecific brood parasitism as a conditional reproductive tactic in the treehopper Publilia concava

In species exhibiting egg guarding as well as communal egg laying, females may adopt the strategy of laying eggs in the nests of conspecifics and leaving without providing care (termed intraspecific brood parasitism). This study is the first to describe such a behavior in the insect Publilia concava (Hemiptera: Membracidae) through field studies that followed 849 marked females across 1,828 brood associations. While brood parasitism increased the total number of eggs in a host brood, it did not reduce the overall hatching success of host broods. Solitary females exhibited a range of guarding durations while parasitic females rarely remained to guard eggs. Females exhibiting the parasitic tactic increased their lifetime number of clutches without decreasing the number of solitary clutches that they were able to initiate. Estimates of egg number for these individual broods revealed that females adopting the parasitic tactic (in addition to solitary breeding) had higher lifetime fecundity relative to females that did not parasitize. In females that exhibited both tactics (solitary and parasitic), the parasitic tactic yielded a higher rate of oviposition. The major component of oviposition rate was the time to find hosts and this time decreased with increasing host availability across 222 replicate groups. Females exhibited a shift toward the parasitic tactic when host broods were more abundant (i.e. in larger groups and later in the season). However, the time to find hosts increased as the frequency of the parasitic tactic increased, suggesting that this tactic may be maintained through negative frequency dependence. The results of this study suggest that brood parasitism may be the preferred tactic, as part of a conditional strategy, when hosts are readily available with solitary breeding being the preferred tactic when hosts are in short supply.

Pollinator Limitation, Autogamy and Minimal Inbreeding Depression in Insect-pollinated Plants on a Boreal Island

Abstract We studied the pollination biology of 18 common insect-pollinated plant species on Kent Island, a boreal island in the Bay of Fundy, New Brunswick, Canada. Under natural conditions, fruit set was relatively high in most of the species studied [although it was very low (<1%) in Maianthemum canadense]. Hand-pollination increased fruit set in five of seven species examined (71%), indicating that fruit set may commonly be limited by the availability or behavior of pollinators on Kent Island. Twelve of 17 species examined (71%) were capable of substantial autonomous self-pollination (autogamy in the absence of pollinators), although fruit set averaged higher in open-pollinated flowers (65.7%) than in flowers from which insects were experimentally excluded (49.6%). The number of seeds per fruit was also less in autonomously self-pollinated flowers in two species (Rhododendron canadense and Ledum groenlandicum). In at least one species (Iris versicolor), rates of autonomous selfing were higher on Kent Island than on the mainland. Stamen-excision experiments in I. versicolor demonstrated that fruit set required pollen transfer in the absence of pollinators (i.e., agamospermy did not occur). In hand-pollination experiments, five of six species (83%) (R. canadense, L. groenlandicum, Smilacina trifolia, S. stellata and I. versicolor) showed no evidence of inbreeding depression in terms of percent fruit set, fruit size or number of seeds per fruit. Overall, our results demonstrate that for many insect-pollinated plant species on Kent Island, pollinators are likely to be limiting, autogamy is common and inbreeding depression is negligible. Although pollinator limitation and autogamy regularly occur in mainland habitats as well, a review of the literature suggests that they may be more common on islands such as Kent Island. If such island-mainland differences are general, they may arise because genotypes and species capable of self-fertilization are more likely than obligate outcrossers to colonize and become established in isolated habitats.

Stage‐dependent feeding behavior by western tarnished plant bugs influences flower bud abscission in cotton

Unexplained variability in the relationship between the number of herbivores in a field and the amount of crop damage can arise if there is a large amount of variation among herbivore individuals in the amount of feeding damage each generates. In California, populations of the western tarnished plant bug, Lygus hesperus Knight (Heteroptera: Miridae), produce highly variable levels of damage to cotton plants (Gossypium hirsutum L.) (Malvaceae), even when found at low densities. Because L. hesperus populations are also highly variable in their overall stage structure, we hypothesize that differences in crop damage might result from varying impact by each L. hesperus stage on cotton flower buds (termed squares). Laboratory measurements of L. hesperus mouth‐parts and distance to anther sacs, a preferred feeding site, revealed that 1st−3rd instar L. hesperus nymphs will not be able to feed on anther sacs of larger squares (over 8 mm in length) but will be able to feed on squares that are most sensitive to L. hesperus damage (<7 mm). Because even the 1st instars can feed on the most sensitive ‘pinhead’ squares, size constraints do not rule out damaging effects from the youngest L. hesperus. Laboratory observations revealed that later developmental stages, and adults, spend more time feeding on cotton squares relative to 2nd and 3rd instars. In addition, a field experiment revealed no effect of 2nd instars on square retention (relative to control cages) but did reveal a significant decrease in square retention generated by adult L. hesperus (4th instar L. hesperus resulted in an intermediate level of square retention). In a final study we sampled L. hesperus stage structure and density across 38 cotton fields. Multiple regression revealed that the densities of 1st−3rd instars of L. hesperus are not correlated with anther sac damage or square retention. However, in 2 years 4th and 5th instars were positively correlated with anther sac damage and negatively correlated with square retention. In the a third year, adult L. hesperus showed correlations in the same direction, across fields and across sites within fields. Overall, these results suggest that the adults and the largest nymphs of L. hesperus (4th and 5th instars) are particularly damaging to cotton squares, with the 1st−3rd instars of L. hesperus causing little damage to plants.

Maternal nest defense reduces egg cannibalism by conspecific females in the maritime earwig Anisolabis maritima

Nest predation imposes a major cost to reproductive females, who should therefore take measures to avoid encounters with predators. However, when predators are conspecifics, avoidance can be more difficult and may be a consequence of social or aggregative behaviors. In this study, we measured the consequences of conspecific egg cannibalism on hatching success in the maritime earwig (Anisolabis maritima), which occasionally form aggregations. We hypothesized that conspecific egg cannibalism is a byproduct of aggregation, and that cannibalism rates would increase with aggregation density; however, our results do not support this. We combined field data with a lab experiment to test the effectiveness of maternal nest defense in protecting nests from a conspecific. Nests with a guard had higher hatching success and lower rates of cannibalism than unattended nests in the presence of a conspecific. We also measured body and forcep size to see whether the outcome of contests was determined by relative size. Female guards who were larger relative to the invading conspecific maintained their nest and had higher hatching success than females who were relatively smaller, suggesting that the maritime earwig is under directional selection for larger body and/or forcep size.

Estimating the Impact of Lygus hesperus on Cotton: The Insect, Plant, and Human Observer as Sources of Variability

Abstract Unexplained variation in the relationship between herbivore densities and the short-term appearance of crop damage is sometimes observed in pest management. Here we used a field survey of commercial cotton fields and a linked questionnaire for cooperating pest control advisors to document the existence of such unexplained variation in the impact of the western tarnished plant bug, Lygus hesperus, on upland cotton, Gossypium hirsutum. L. hesperus feeds preferentially on flower buds (“squares”), and the plant may respond to this damage with abscission of the square. We explored four classes of factors that might contribute to unexplained variation in square abscission. First, misperceptions by the human observer (i.e., sampling problems) may play a role, because commercial field scouts significantly underestimate densities of L. hesperus nymphs. Second, we found no support for the hypothesis that variable behavior expressed by L. hesperus contributes to unexplained variation in square abscission. L. hesperus seems to generate relatively predictable levels of square feeding damage; the variation that was observed was unrelated to grower categorization of fields as exhibiting normal versus unexpectedly high or low levels of square abscission. Third, variable plant responses to damage may instead be the key source of unexplained square abscission. Younger plants and plants with higher petiole phosphate concentrations expressed increased sensitivity to L. hesperus feeding; these correlations must, however, be tested experimentally before definitive conclusions are drawn. Fourth, another arthropod might be generating damage that was erroneously being attributed to L. hesperus. The omnivore Geocoris pallens was a candidate agent of cryptic damage to squares; however, an experiment showed that G. pallens generated only trivial square damage and no detectable increase in square abscission. Thus, this study has focused our attention away from the arthropod side of the interaction and toward the host plant as the primary source of greater than expected square abscission generated by L. hesperus.

State‐dependent sampling bias in insects: implications for monitoring western tarnished plant bugs

Insect populations vary in the proportion of individuals exhibiting a particular ‘state’ (e.g., developmental stage, sex, egg load, or nutritional status). Because an insects developmental state often determines both its size and its behavior, it is likely that this will also affect the probability of being sampled. We propose that a comprehensive approach to pest management must consider the interaction between the structure of a pest population (i.e., the relative number of individuals in each state) and any state‐dependent sampling bias. To illustrate the usefulness of this method we sampled populations of the western tarnished pest bug, Lygus hesperus Knight (Heteroptera: Miridae), in cotton fields. Our sampling technique utilized large cages to measure the absolute densities of each L. hesperus stage and adult sex within a population. This technique allowed us to document a wide range of absolute stage structures and sex ratios across 10 L. hesperus populations in California. Using a combination of cage samples and sweep net samples, we quantified the state‐dependent sampling bias by calculating the efficiency of sweep sampling as a function of L. hesperus developmental stage and sex. We found that the efficiency of sweep nets increased steadily with each successive developmental stage (i.e., nymphal instar) of L. hesperus. We also found that sweep nets are slightly more efficient in capturing male vs. female L. hesperus adults. Since other studies have documented that the stage and sex of L. hesperus can affect feeding impact on cotton flower buds, our results suggest that accurate predictions of Lygus damage will need to incorporate stage and sex‐dependent sampling biases.

Stage-specific predation on Lygus hesperus affects its population stage structure

Evidence suggests that prey can vary in their susceptibility to predation depending on their developmental stage. Stage‐dependent predation is of particular importance to integrated pest management, because it is often a particular developmental stage of a pest that causes the majority of the damage to the crop. An understanding of stage‐dependent biocontrol is therefore important for predicting the ultimate impact of herbivore populations. In this article, we addressed this issue by focusing on the stage structure of Lygus hesperus Knight (Heteroptera: Miridae) populations in cotton as related to the density of a specific generalist predator. We first demonstrated in a field experiment that Geocoris spp. adults suppressed L. hesperus eggs and/or early instars (first through third), but did not suppress fourth through fifth instars or adult L. hesperus. We then demonstrated that this stage‐specific predation translated into season‐long shifts in the stage structure of L. hesperus populations in cotton fields. Using weekly sweep counts across 21 separate cotton fields, we found a negative correlation between season‐long Geocoris spp. densities and season‐long densities of L. hesperus nymphs. In contrast, there was no such correlation between Geocoris spp. and L. hesperus adults. Taken together, these results suggest that Geocoris spp. predators influence the stage structure of L. hesperus populations in cotton, which in turn has the potential to affect patterns of cotton square damage and sampling bias when monitoring L. hesperus populations.

Evolution of conspecific brood parasitism versus cooperative breeding as alternative reproductive tactics

Cooperative breeding and conspecific brood parasitism can both be favored by ecological saturation of breeding territories or nest sites. Here, we develop a model that links these alternative reproductive tactics by focusing on nonnesting females (S) that either breed cooperatively with a nesting female (N) or parasitize a third, outside host female (H). We find that cooperative breeding is more likely to evolve with increasing relatedness of cooperating females (S or N) to the outside host female (H) and with increasing costs to the hosts for receiving parasitic eggs. Conversely, cooperation is less likely with increasing kinship between the two potentially cooperative nesters (S and N). This is because even the nesting female gains higher inclusive fitness as long as the number of parasitic eggs (of her otherwise potentially cooperating partner) is sufficiently high. We find the relationship between kinship and reproductive skew within cooperative nests can be either positive or negative depending on the fecundity of parasites versus nesting females. We also find that either of the cooperatively nesting females is more likely to tolerate a smaller fraction of group reproduction as kinship with the host female increases and as the host reproduces more (relative to the parasite) in outside nests. Finally, our model predicts that, as the outside option of conspecific brood parasitism becomes more profitable, helping behavior (zero reproduction by one female) is less likely to evolve in cooperatively breeding groups.

Synthesizing perspectives on the evolution of cooperation within and between species

Cooperation is widespread both within and between species, but are intraspecific and interspecific cooperation fundamentally similar or qualitatively different phenomena? This review evaluates this question, necessary for a general understanding of the evolution of cooperation. First, we outline three advantages of cooperation relative to noncooperation (acquisition of otherwise inaccessible goods and services, more efficient acquisition of resources, and buffering against variability), and predict when individuals should cooperate with a conspecific versus a heterospecific partner to obtain these advantages. Second, we highlight five axes along which heterospecific and conspecific partners may differ: relatedness and fitness feedbacks, competition and resource use, resource‐generation abilities, relative evolutionary rates, and asymmetric strategy sets and outside options. Along all of these axes, certain asymmetries between partners are more common in, but not exclusive to, cooperation between species, especially complementary resource use and production. We conclude that cooperation within and between species share many fundamental qualities, and that differences between the two systems are explained by the various asymmetries between partners. Consideration of the parallels between intra‐ and interspecific cooperation facilitates application of well‐studied topics in one system to the other, such as direct benefits within species and kin‐selected cooperation between species, generating promising directions for future research.