David H. Hembry

Coevolution and the diversification of life.

Coevolution, reciprocal adaptation between two or more taxa, is commonly invoked as a primary mechanism responsible for generating much of Earth’s biodiversity. This conceptually appealing hypothesis is incredibly broad in evolutionary scope, encompassing diverse patterns and processes operating over timescales ranging from microbial generations to geological eras. However, we have surprisingly little evidence that large-scale associations between coevolution and diversity reflect a causal relationship at smaller timescales, in which coevolutionary selection is directly responsible for the formation of new species. In this synthesis, we critically evaluate evidence for the often-invoked hypothesis that coevolution is an important process promoting biological diversification. We conclude that the lack of widespread evidence for coevolutionary diversification may be best explained by the fact that coevolution’s importance in diversification varies depending on the type of interaction and the scale of the diversification under consideration.

Non-congruent colonizations and diversification in a coevolving pollination mutualism on oceanic islands.

A challenge for coevolutionary theory is how different types of interaction influence the diversification of coevolving clades. Reciprocal specialization is characteristic of certain coevolving, mutualistic interactions, but whether this specialization seen in ecological time constrains changes in patterns of interaction over evolutionary time remains unclear. Here, we examine the co-radiation of Glochidion trees (Phyllanthaceae: Phyllanthus s. l.) and pollinating, seed-predatory Epicephala moths (Lepidoptera: Gracillariidae) on young (mostly later than 5 Ma) oceanic islands in southeastern Polynesia. Epicephala are the sole known pollinators of Glochidion trees, and show extreme reciprocal specialization in continental Asia. We find that Glochidion and Epicephala diversified across these islands through repeated, non-congruent colonizations, and that one recently colonizing Epicephala lineage has spread across 12 host species in three archipelagos in less than 1 Myr. These results indicate that reciprocal specialization and coadaptation do not prevent dramatic changes in associations between intimately associated taxa over short evolutionary time scales. Not only are these host associations more dynamic than previously recognized, but these changes in patterns of interaction may play an important role in the diversification of coevolving taxa.

Repeated colonization of remote islands by specialized mutualists

Mutualisms are ubiquitous in nature, but constraints imposed by specialization may limit their ability to colonize novel environments synchronously. The ability of mutualisms to reassemble following disturbance is central to understanding their response to global change. Here, we demonstrate that a highly specialized pollination mutualism considered to be obligate (Phyllanthaceae: Glochidion; Lepidoptera: Gracillariidae: Epicephala) has colonized some of the worlds most isolated archipelagoes, and we record, to our knowledge, for the first time the presence of Epicephala moths from 19 host Glochidion species on 17 islands in the Pacific Ocean. Our findings appear to offer a remarkable example of mutualism persistence in an insect–plant interaction characterized by reciprocal specialization and mutual dependence. These findings also appear to contradict the island biogeography paradigm that taxa with specialized biotic interactions are unlikely to colonize oceanic islands.

Conflicting Selection in the Course of Adaptive Diversification: The Interplay between Mutualism and Intraspecific Competition

Adaptive speciation can occur when a population undergoes assortative mating and disruptive selection caused by frequency-dependent intraspecific competition. However, other interactions, such as mutualisms based on trait matching, may generate conflicting selective pressures that constrain species diversification. We used individual-based simulations to explore how different types of mutualism affect adaptive diversification. A magic trait was assumed to simultaneously mediate mate choice, intraspecific competition, and mutualisms. In scenarios of intimate, specialized mutualisms, individuals interact with one or few individual mutualistic partners, and diversification is constrained only if the mutualism is obligate. In other scenarios, increasing numbers of different partners per individual limit diversification by generating stabilizing selection. Stabilizing selection emerges from the greater likelihood of trait mismatches for rare, extreme phenotypes than for common intermediate phenotypes. Constraints on diversification imposed by increased numbers of partners decrease if the trait matching degree has smaller positive effects on fitness. These results hold after the relaxation of various assumptions. When trait matching matters, mutualism-generated stabilizing selection would thus often constrain diversification in obligate mutualisms, such as ant-myrmecophyte associations, and in low-intimacy mutualisms, including plant-seed disperser systems. Hence, different processes, such as trait convergence favoring the incorporation of nonrelated species, are needed to explain the higher richness of low-intimacy assemblages—shown here to be up to 1 order of magnitude richer than high-intimacy systems.

Why do ants shift their foraging from extrafloral nectar to aphid honeydew

When aphids parasitize plants with extrafloral nectaries (EFNs) and aphid colony size is small, ants frequently use EFNs but hardly tend aphids. However, as the aphid colony size increases, ants stop using EFNs and strengthen their associations with aphids. Although the shift in ant behavior is important for determining the dynamics of the ant–plant–aphid interaction, it is not known why this shift occurs. Here, we test two hypotheses to explain the mechanism responsible for this behavioral shift: (1) Extrafloral nectar secretion changes in response to aphid herbivory, or (2) plants do not change extrafloral nectar secretion, but the total reward to ants from aphids will exceed that from EFNs above a certain aphid colony size. To judge which mechanism is plausible, we investigated secretion patterns of extrafloral nectar produced by plants with and without aphids, compared the amount of sugar supplied by EFNs and aphids, and examined whether extrafloral nectar or honeydew was more attractive to ants. Our results show that there was no inducible extrafloral secretion in response to aphid herbivory, but the sugar concentration in extrafloral nectar was higher than in honeydew, and more ant workers were attracted to an artificial extrafloral nectar solution than to an artificial aphid honeydew solution. These results indicate that extrafloral nectar is a more attractive reward than aphid honeydew per unit volume. However, even an aphid colony containing only two individuals can supply a greater reward to ants than EFNs. This suggests that the ant behavioral shift may be explained by the second hypothesis.

A Novel, Enigmatic Basal Leafflower Moth Lineage Pollinating a Derived Leafflower Host Illustrates the Dynamics of Host Shifts, Partner Replacement, and Apparent Coadaptation in Intimate Mutualisms

Leafflower plant/leafflower moth brood pollination mutualisms are widespread in the Paleotropics. Leafflower moths pollinate leafflower plants, but their larvae consume a subset of the hosts’ seeds. These interactions are highly phylogenetically constrained: six clades of leafflower plants are each associated with a unique clade of leafflower moths (Epicephala). Here, we report a previously unrecognized basal seventh pollinating Epicephala lineage—associated with the highly derived leafflower clade Glochidion—in Asia. Epicephala lanceolaria is a pollinator and seed predator of Glochidion lanceolarium. Phylogenetic inference indicates that the ancestor of E. lanceolaria most likely shifted onto the ancestor of G. lanceolarium and displaced the ancestral allospecific Epicephala pollinator in at least some host populations. The unusual and apparently coadapted aspects of the G. lanceolarium/E. lanceolaria reproductive cycles suggest that plant-pollinator coevolution may have played a role in this displacement and provide insights into the dynamics of host shifts and trait coevolution in this specialized mutualism.

Phyllantheae–Epicephala Mutualistic Interactions on Oceanic Islands in the Pacific

Oceanic islands, and the organisms that live on them, have long served as models for the study of evolution. Formed de novo by volcanism or by the uplift of previously submerged rock, oceanic islands have never been connected to continents. They are colonized by a limited number of founding lineages that arrive via long-distance dispersal. The resulting discrete and isolated nature of these communities and the organisms within them have led oceanic islands to be used as “natural laboratories” since the time of Darwin by researchers interested in speciation (Darwin 1859; Coyne and Orr 2004; Goodman et al. 2012), adaptive radiation (Lack 1947; Carlquist 1974; Chiba 2004; Grant and Grant 2008), and community assembly (MacArthur and Wilson 1967; Gillespie 2004; Casquet et al. 2015). The utility of oceanic island biotas as models for evolutionary insights is indicated by their ongoing adoption in new areas of evolutionary ecology, such as diversification dynamics (Economo and Sarnat 2012; Bennett and O’Grady 2013), host–microbe interactions (Ort et al. 2012, O’Connor et al. 2014), and coevolutionary biology (Hembry et al. 2013a).

Herbarium Specimens Reveal Putative Insect Extinction on the Deforested Island of Mangareva (Gambier Archipelago, French Polynesia)

Abstract: Human activities are expected to result in extinction of many organisms in taxonomically neglected lineages; however, actually documenting these extinctions is very difficult for soft-bodied organisms that do not leave a subfossil record. Subfossil and historic records reveal that human-induced extinction has been particularly marked for gastropods and terrestrial vertebrates on Pacific islands, but whether human activities resulted in similar biodiversity loss in soft-bodied, taxonomically neglected animals (such as insects) remains unclear. However, in cases in which specialized plant-feeding insects leave diagnostic feeding damage on plants, herbarium specimens coupled with resurvey efforts may indicate potential extinctions or extirpations during historic times. Here, I report the discovery of leaf mines in herbarium specimens of the plant Phyllanthus wilderi (Phyllanthaceae: Glochidion sensu lato) from the island of Mangareva (Gambier Islands, French Polynesia). These mines were not rediscovered in recent surveys on Mangareva but are similar to those made today by leaf-mining moths (Lepidoptera: Gracillariidae) on many other islands in southeastern Polynesia. This is, to the best of my knowledge, the first report of a potential insect extinction from Mangareva, an island already well known for its history of anthropogenic habitat destruction and biodiversity loss. This result indicates that herbarium specimens may be used to identify potentially extinct and extirpated insect taxa. Future biodiversity surveys on Pacific islands and elsewhere should use herbarium specimens as a guide both to documenting potential extinctions and to search for rediscovery of rare taxa.

Analysing ecological networks of species interactions.

Network approaches to ecological questions have been increasingly used, particularly in recent decades. The abstraction of ecological systems – such as communities – through networks of interactions between their components indeed provides a way to summarize this information with single objects. The methodological framework derived from graph theory also provides numerous approaches and measures to analyze these objects and can offer new perspectives on established ecological theories as well as tools to address new challenges. However, prior to using these methods to test ecological hypotheses, it is necessary that we understand, adapt, and use them in ways that both allow us to deliver their full potential and account for their limitations. Here, we attempt to increase the accessibility of network approaches by providing a review of the tools that have been developed so far, with – what we believe to be – their appropriate uses and potential limitations. This is not an exhaustive review of all methods and metrics, but rather, an overview of tools that are robust, informative, and ecologically sound. After providing a brief presentation of species interaction networks and how to build them in order to summarize ecological information of different types, we then classify methods and metrics by the types of ecological questions that they can be used to answer from global to local scales, including methods for hypothesis testing and future perspectives. Specifically, we show how the organization of species interactions in a community yields different network structures (e.g., more or less dense, modular or nested), how different measures can be used to describe and quantify these emerging structures, and how to compare communities based on these differences in structures. Within networks, we illustrate metrics that can be used to describe and compare the functional and dynamic roles of species based on their position in the network and the organization of their interactions as well as associated new methods to test the significance of these results. Lastly, we describe potential fruitful avenues for new methodological developments to address novel ecological questions.

Effects of anthropogenic wildfire in low-elevation Pacific island vegetation communities in French Polynesia

Anthropogenic (or human-caused) wildfire is an increasingly important driver of ecological change on Pacific islands including southeastern Polynesia, but fire ecology studies are almost completely absent for this region. Where observations do exist, they mostly represent descriptions of fire effects on plant communities before the introduction of invasive species in the modern era. Understanding the effects of wildfire in southeastern Polynesian island vegetation communities can elucidate which species may become problematic invasives with continued wildfire activity. We investigate the effects of wildfire on vegetation in three low-elevation sites (45–379 m) on the island of Mo’orea in the Society Islands, French Polynesia, which are already heavily impacted by past human land use and invasive exotic plants, but retain some native flora. In six study areas (three burned and three unburned comparisons), we placed 30 transects across sites and collected species and abundance information at 390 points. We analyzed each local community of plants in three categories: natives, those introduced by Polynesians before European contact (1767 C.E.), and those introduced since European contact. Burned areas had the same or lower mean species richness than paired comparison sites. Although wildfire did not affect the proportions of native and introduced species, it may increase the abundance of introduced species on some sites. Non-metric multidimensional scaling indicates that (not recently modified) comparison plant communities are more distinct from one another than are those on burned sites. We discuss conservation concerns for particular native plants absent from burned sites, as well as invasive species (including Lantana camara and Paraserianthes falcataria) that may be promoted by fire in the Pacific.