Phylogenetic structure of specialization: A new approach that integrates partner availability and phylogenetic diversity to quantify biotic specialization in ecological networks

Abstract

Biotic specialization holds information about the assembly, evolution, and stability of biological communities. Partner availabilities can play an important role in enabling species interactions, where uneven partner availabilities can bias estimates of biotic specialization when using phylogenetic diversity indices. It is therefore important to account for partner availability when characterizing biotic specialization using phylogenies. We developed an index, phylogenetic structure of specialization (PSS), that avoids bias from uneven partner availabilities by uncoupling the null models for interaction frequency and phylogenetic distance. We incorporate the deviation between observed and random interaction frequencies as weights into the calculation of partner phylogenetic α‐diversity. To calculate the PSS index, we then compare observed partner phylogenetic α‐diversity to a null distribution generated by randomizing phylogenetic distances among the same number of partners. PSS quantifies the phylogenetic structure (i.e., clustered, overdispersed, or random) of the partners of a focal species. We show with simulations that the PSS index is not correlated with network properties, which allows comparisons across multiple systems. We also implemented PSS on empirical networks of host–parasite, avian seed‐dispersal, lichenized fungi–cyanobacteria, and hummingbird pollination interactions. Across these systems, a large proportion of taxa interact with phylogenetically random partners according to PSS, sometimes to a larger extent than detected with an existing method that does not account for partner availability. We also found that many taxa interact with phylogenetically clustered partners, while taxa with overdispersed partners were rare. We argue that species with phylogenetically overdispersed partners have often been misinterpreted as generalists when they should be considered specialists. Our results highlight the important role of randomness in shaping interaction networks, even in highly intimate symbioses, and provide a much‐needed quantitative framework to assess the role that evolutionary history and symbiotic specialization play in shaping patterns of biodiversity. PSS is available as an R package at https://github.com/cjpardodelahoz/pss .

Phylogenetic relatedness of food plants reveals highest insect herbivore specialization at intermediate temperatures along a broad climatic gradient

“…The phylogeny‐based specialization depends on the phylogenetic structure of resources and resource availability. Based on the relationship between the phylogenetic α ‐diversity of plant assemblages and the phylogeny‐based specialization index, we conclude that the phylogenetic structure of plant assemblages also shaped specialization patterns along our sampled climatic gradient (Pardo‐De la Hoz et al, 2022). We detected wide diet breadths of herbivores at cold and warm sites, respectively.…”

“…The analysis of d’ of widespread species along the gradient revealed increasing specialization with temperature, suggesting that intraspecific changes could contribute to more specialized networks in warm habitats. As evidence of specialization patterns along environmental gradients is conflicting, the inclusion of phylogenetic relationships and resource availability can help to disentangle patterns and underlying processes of biotic specialization of mobile, generalist herbivore taxa such as Orthoptera in ecological networks (Jorge et al, 2017; Pardo‐De la Hoz et al, 2022).…”

“…( DSI* values for all sampled species in our study are provided in Table S3). Combining d’ and phylogenetic α ‐diversity of resources by decoupling the null models for interaction frequency and phylogenetic distance, we also computed the phylogenetic structure of specialization ( PSS ) as an alternative improved measure for herbivore specialization (see supplementary methods, Pardo‐De la Hoz et al, 2022).…”

“…Recent advances in calculating resource specialization of herbivores were proposed by Jorge et al (2017) and Pardo‐De la Hoz et al (2022). Rather than using counts of resource species or higher taxonomic categories to measure diet breadths of herbivores, the rescaled standardized distance‐based specialization index ( DSI* ) weighs the degree of specialization by the phylogenetic similarity of resources and accounts for their availability.…”

“…Regardless of the number of plant species in the diet of a phytophagous insect, its dietary niche breadth is also determined by characteristics of the ingested resources, as plants differ in their costs and gains of use. Since phylogenetically related taxa often share similar traits (Goberna & Verdú, 2016; Swenson, 2014; Swenson & Enquist, 2007), phylogenetic distances can be interpreted as an integration of plant traits such as chemical defenses and mechanical properties and, thereby, estimate the trait‐based dietary niche breadth of herbivore species (Jorge et al, 2017; Pardo‐De la Hoz et al, 2022; Rasmann & Agrawal, 2011). Thus, measuring specialization levels of herbivores requires the inclusion of functional traits or phylogenetic relationships for a more realistic assessment of its niche breadth (Jorge et al, 2017; Pardo‐De la Hoz et al, 2022).…”