John N. Thompson’s research while affiliated with University of California, Santa Cruz and other places

Indirect effects shape many aspects of our day to day life. While in social networks indirect effects drive our opinion and behaviour, in economical networks they affect the interdependence among global markets, and in contact networks they drive how contagious diseases spread. In this study we show that indirect effects can also shape one of the major currencies in biology: fitness. We show that the fitness of species that mutually benefit each other and interact in mutualistic networks is driven by indirect evolutionary effects, with important consequences for how species respond to perturbations, for instance, when an alien species is introduced in the network.

Coevolution has the potential to alter not only the ecological interactions of coevolving partners, but also their interactions with yet other species. The effects of coevolution may ripple throughout networks of interacting species, cascading across trophic levels, swamping competitors, or facilitating survival or reproduction of yet other species linked only indirectly to the coevolving partners. These ripple effects of coevolution may differ among communities, amplifying how the coevolutionary process produces geographic mosaics of traits and outcomes in interactions among species. In a From the Cover article in this issue of Molecular Ecology, Hague et al. (2022) provide a clear example, using the well-studied interactions between Pacific newts (Taricha spp.) and their common garter snake (Thamnophis sirtalis) predators in western North America. Pacific newts harbour tetrodotoxin (TTX), which is highly toxic to vertebrate predators. In coevolutionary hotspots, extreme escalation of toxicity in the newts and resistance to toxicity in the snakes have resulted in snake populations that retain high levels of TTX. In two geographic regions, snakes in these hotspot populations have evolved bright, aposematic colours that may act as warning signals to their own vertebrate predators. The warning signals and toxin-resistance alleles in the snake populations decrease clinally away from the coevolutionary hotpots, shaped by a geographically variable mix of selection imposed by the snakes' prey and by their own predators.

Selection leading to adaptation to interactions may generate rapid evolutionary feedbacks and drive diversification of species interactions. The challenge is to understand how the many traits of interacting species combine to shape local adaptation in ways directly or indirectly resulting in diversification. We used the well‐studied interactions between Lithophragma plants (Saxifragaceae) and Greya moths (Prodoxidae) to evaluate how plants and moths together contributed to local divergence in pollination efficacy. Specifically, we studied L. bolanderi and its two specialized Greya moth pollinators in two contrasting environments in the Sierra Nevada in California. Both moths pollinate L. bolanderi during nectaring, one of them–G. politella–also while ovipositing through the floral corolla into the ovary. First, field surveys of floral visitors and the presence of G. politella eggs and larvae in developing capsules showed that one population was visited only by G. politella and few other pollinators, whereas the other was visited by both Greya species and other pollinators. Second, L. bolanderi in these two natural populations differed in several floral traits putatively important for pollination efficacy. Third, laboratory experiments with greenhouse‐grown plants and field‐collected moths showed that L. bolanderi was more efficiently pollinated by local compared to nonlocal nectaring moths of both species. Pollination efficacy of ovipositing G. politella was also higher for local moths for the L. bolanderi population, which relies more heavily on this species in nature. Finally, time‐lapse photography in the laboratory showed that G. politella from different populations differed in oviposition behavior, suggesting the potential for local adaptation also among Greya populations. Collectively, our results are a rare example of components of local adaptation contributing to divergence in pollination efficacy in a coevolving interaction and, thus, provide insights into how geographic mosaics of coevolution may lead to coevolutionary diversification in species interactions.

In this remembrance, we have brought together some of Victor Rico‐Gray’s friends and collaborators to recall his many contributions to tropical ecology and his influence on so many young scientists. Victor’s research ranged from Mexican ethnobotany to the evolutionary ecology of complex interactions between ants and plants. His research was highly collaborative, forming strong bonds among those who shared his interests in how the web of life is organized. He inspired students through his mentoring in tropical ecology, mainly his lectures at the Instituto de Ecología AC (INECOL), and later at the Universidad Veracruzana (UV), his courses organized by the Organization for Tropical Studies (OTS), and his talks at meetings, including the Association of Tropical Biology and Conservation (ATBC). Victor’s story is not over. It will continue to be traced through countless scientists who were inspired by Victor’s life and work. We started by describing the Victor's life and his graduate studies in tropical ecology. Next, we highlight the Victor's importance in the formation of new scientists and in tropical ecology. We finished the text by gathering good memories and anecdotes of Victor.

Volatiles are of key importance for host-plant recognition in insects. In the pollination system of Lithophragma flowers and Greya moths, moths are highly specialized on Lithophragma, in which they oviposit and thereby pollinate the flowers. Floral volatiles in Lithophragma are highly variable between species and populations, and moths prefer to oviposit into Lithophragma flowers from populations of the local host species. Here we used gas chromatography coupled with electroantennographic detection (GC-EAD) to test whether Greya moths detect specific key volatiles or respond broadly to many volatiles of Lithophragma flowers. We also addressed whether olfactory detection in Greya moths varies across populations, consistent with a co-evolutionary scenario. We analyzed flower volatile samples from three different species and five populations of Lithophragma occurring across a 1400 km range in the Western USA, and their sympatric female Greya politella moths. We showed that Greya politella detect a broad range of Lithophragma volatiles, with a total of 23 compounds being EAD active. We chemically identified 15 of these, including the chiral 6, 10, 14-trimethylpentadecan-2-one (hexahydrofarnesyl acetone), which was not previously detected in Lithophragma. All investigated Lithophragma species produced the (6R, 10R)-enantiomer of this compound. We showed that Greya moths detected not only volatiles of their local Lithophragma plants, but also those from allopatric populations/species that they not encounter in local populations. In conclusion, the generalized detection of volatiles and a lack of co-divergence between volatiles and olfactory detection may be of selective advantage for moths in tracking hosts with rapidly evolving, chemically diverse floral volatiles.

Ecological interactions shape the evolution of multiple species traits in populations. These traits are often linked to each other through genetic correlations, affecting how each trait evolves through selection imposed by interacting partners. Here, we integrate quantitative genetics, coevolutionary theory and network science to explore how trait correlations affect the coevolution of mutualistic species not only in pairs of species but also in species-rich networks across space. We show that genetic correlations may determine the pace of coevolutionary change, affect species abundances and fuel divergence among populations of the same species. However, this trait divergence promoted by genetic correlations is partially buffered by the nested structure of species-rich mutualisms. Our study, therefore, highlights how coevolution and its ecological consequences may result from conflicting processes at different levels of organisation, ranging from genes to communities.

The spatial distribution of populations can influence the evolutionary outcome of species inter- actions. The variation in direction and strength of selection across local communities creates geographic selection mosaics that, when combined with gene flow and genomic processes such as genome duplication or hybridization, can fuel ongoing coevolution. A fundamental prob- lem to solve is how coevolution proceeds when many populations that vary in their ecological outcomes are connected across large landscapes. Here we use a lattice model to explore this problem. Our results show that the complex interrelationships among the elements of the geo- graphic mosaic of coevolution can lead to the formation of clusters of populations with similar phenotypes that are larger than expected by local selection. Our results indicate that neither the spatial distribution of phenotypes nor the spatial differences in magnitude and direction of selection alone dictate coevolutionary dynamics: the geographic mosaic of coevolution affects formation of phenotypic clusters, which in turn affect the spatial and temporal dynamics of co- evolution. Because the formation of large phenotypic clusters depends on gene flow, we predict current habitat fragmentation will change the outcomes of geographic mosaics, coupling spatial patterns in selection and phenotypes.

Significance A major challenge in biology is to understand how complex traits important for ecological interactions between species coevolve and diversify across contrasting ecosystems. Floral scents are complex, and are often composed of a diverse array of chemicals important for interactions between plants and pollinators, herbivores, and microbial symbionts. We studied diversification of floral scents among populations of all woodland star species ( Lithophragma ) across far-western North America. Floral scent variation was structured not only phylogenetically among species and geographically among populations, but some of the divergence was driven by local differences in the presence of coevolved Greya moth pollinators. These results highlight the importance of conserving multiple populations of species if we are to maintain the evolutionary potential of coevolving interactions.

Significance The reciprocal evolution of interacting species, or coevolution, generates impressive adaptations in pairs of species across geographic regions. However, we currently do not understand how coevolution shapes adaptations in large groups of species that interact not just locally but also across ecosystems. We use a mathematical model of coevolution and network tools to show that gene flow resulting from movement of individuals among populations may favor, rather than swamp, reciprocal adaptation in mutualisms, especially in large and heterogeneous networks typical of pollination and seed dispersal interactions. Our results suggest that the disruption of gene flow, fueled by human activities, may undermine long-term adaptation in mutualistic assemblages, with severe consequences for the functioning of ecological systems.