Competition and hybridization drive interspecific territoriality in birds Jonathan P. Drurya,1, Madeline C. Cowenb, and Gregory F. Gretherb aDepartment of Biosciences, Durham University, DH1 3LE Durham, United Kingdom; and bDepartment of Ecology & Evolutionary Biology, University of California, Los Angeles, CA 90095 Edited by Jonathan B. Losos, Washington University in St. Louis, St. Louis, MO, and approved April 13, 2020 (received for review December 5, 2019) Costly interactions between species that arise as a by-product of recent for divergent agonistic character displacement to have oc- ancestral similarities in communication signals are expected to curred or selection has been too weak to overcome gene flow from persist only under specific evolutionary circumstances. Territorial allopatry (16, 17). Conversely, if the species occupy similar eco- aggression between species, for instance, is widely assumed to logical niches and compete for common resources (e.g., food, persist only when extrinsic barriers prevent niche divergence or nesting sites), interspecific territoriality could be maintained or selection in sympatry is too weak to overcome gene flow from evolve de novo through convergent agonistic character displace- allopatry. However, recent theoretical and comparative studies ment, because partitioning space with competitors is adaptive (2, have challenged this view. Here we present a large-scale, phylo- 9, 15, 23). The classic view is that adaptive interspecific territori- genetic analysis of the distribution and determinants of interspe- ality should only persist when ecological character displacement is cific territoriality. We find that interspecific territoriality is blocked by extrinsic barriers to niche divergence, such as struc- widespread in birds and strongly associated with hybridization turally simple habitats (15). But interspecific territoriality itself and resource overlap during the breeding season. Contrary to causes spatial niche partitioning, which weakens selection for the view that territoriality only persists between species that further niche divergence (24), and therefore could be an evolu- rarely breed in the same areas or where niche divergence is con- tionarily stable alternative to ecological character displacement strained by habitat structure, we find that interspecific territorial- (9). Interspecific mate competition arising from reproductive in- ity is positively associated with breeding habitat overlap and terference could also make interspecific territoriality adaptive if unrelated to habitat structure. Furthermore, our results provide individuals that defend space against heterospecifics have higher EVOLUTION compelling evidence that ancestral similarities in territorial signals reproductive success than those that do not (19, 25–27). The age are maintained and reinforced by selection when interspecific ter- of interacting lineages (i.e., time since the most recent common ritoriality is adaptive. The territorial signals linked to interspecific ancestor) also has an important bearing on the types of in- territoriality in birds depend on the evolutionary age of interact- terspecific interactions likely to be observed (28). Maladaptive ing species, plumage at shallow (within-family) timescales, and song at deeper (between-family) timescales. Evidently, territorial interspecific territoriality and adaptive interspecific territoriality interactions between species have persisted and shaped pheno- maintained by interspecific mate competition should primarily be typic diversity on a macroevolutionary timescale. restricted to closely related species that are phenotypically similar owing to sharing a recent ancestor (29) (e.g., species belonging to behavioral interference | interference competition | phylogenetic comparative methods | Passerines Significance nterspecific territoriality is among the most common forms of Historically, aggressive territorial interactions between mem- Iinterference competition in animals (1–4), and has been shown bers of different species have been dismissed as relatively rare to affect species range (5–8) and drive phenotypic evolution, occurrences and unimportant selective forces. We conducted particularly of traits involved in competitor recognition (9–14). the largest-ever comparative study of interspecific territorial Yet, interspecific territoriality itself remains poorly studied. behavior, amassing a dataset of all published observations of While it is generally logical to infer that at least one individual territorial aggression between species of North American benefits in common within-species interactions, this logic does perching birds. We found that interspecific territoriality is not hold when the individuals are members of different species. common, with individuals from nearly a third of all species The reason is that interspecific territoriality can arise simply as a defending territories against one or more other species. Con- by-product of intraspecific territoriality when species with similar trary to the prevailing view, we also found abundant support territorial signals (e.g., song, coloration, scent marks) first come for the hypothesis that interspecific territoriality is an adaptive response to resource competition and reproductive in- into secondary contact (15–17). Is interspecific territoriality terference, not just a rare occurrence restricted to recently di- merely a nuisance interaction that sometimes prevents species verged lineages, and that interspecific territoriality constrains from coexisting? Or does it instead stabilize coexistence by con- the evolutionary divergence of territorial signals. ferring the same benefits that territoriality does within species? Based on its history of neglect in both ecology and evolutionary Author contributions: J.P.D., M.C.C., and G.F.G. designed research; J.P.D., M.C.C., and biology, one might infer the former, but research on this topic has G.F.G. performed research; J.P.D. and G.F.G. analyzed data; and J.P.D., M.C.C., and surged in recent years, and the hypothesis that interspecific ter- G.F.G. wrote the paper. ritoriality is usually adaptive is gaining traction (9, 18–21). The authors declare no competing interest. In theory, whether interspecific territoriality persists on an This article is a PNAS Direct Submission. evolutionary timescale depends on several factors. If the species Published under the PNAS license. occupy distinctly different ecological niches, selection would Data deposition: All data and code are available at https://github.com/jonathanpdrury/ ordinarily cause them to diverge in territorial signals and com- intersp_territoriality_in_passerines. petitor recognition until interspecific territoriality is eliminated 1To whom correspondence may be addressed. Email: [email protected]. (22), an evolutionary process known as divergent agonistic char- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ acter displacement (4, 9). Maladaptive interspecific territoriality doi:10.1073/pnas.1921380117/-/DCSupplemental. could persist into the present, however, if secondary contact is too First published May 26, 2020. www.pnas.org/cgi/doi/10.1073/pnas.1921380117 PNAS | June 9, 2020 | vol. 117 | no. 23 | 12923–12930 Downloaded by guest on September 26, 2021 the same family). We would only expect to see interspecific ter- We also found strong support for the hypothesis that in- ritoriality between distantly related species if they compete for terspecific territoriality is an adaptive response to interspecific common limiting resources. mate competition (19, 25, 26). Hybridizing species were more One way of tackling these questions is to take a comparative likely to be interspecifically territorial than nonhybridizing spe- approach and ask which of the factors provided here helps ex- cies (Fig. 2D). The relationship between hybridization and plain why some species pairs are interspecifically territorial while interspecific territoriality exists even after controlling for others do not. Thus far, comparative studies of this sort have phenotypic similarity and patristic distance, bolstering support been relatively small in scale (18, 19, 28), and no previous studies for the hypothesis that reproductive interference, per se, pro- have had sufficient phylogenetic depth to evaluate whether dif- motes the evolutionary maintenance of interspecific territorial- ferent types of interspecific territoriality prevail at different ity. Moreover, a statistical interaction between syntopy and taxonomic or evolutionary time scales. We undertook the largest hybridization indicates that hybridizing species tend to be phylogenetic analysis of interspecific territoriality to date, interspecifically territorial regardless of the degree of overlap in amassing a database of 175 reports of interspecific territorial breeding habitat, while nonhybridizing species are much more aggression in North American perching birds (Passeriformes). likely to be interspecifically territorial if they are highly syntopic We focused on this taxon and geographic region primarily be- (Fig. 2D and SI Appendix, Tables S3 and S4). Therefore, hy- cause of the rich literature on avian behavioral ecology and the bridization is an important predictor of interspecific territorial- availability of fine-scale biogeographical data (30). We searched ity, even for species pairs with relatively low breeding habitat all available sources and classified species pairs with multiple overlap.