Carryover effects drive competitive dominance in spatially structured environments Benjamin G. Van Allena,b,1 and Volker H. W. Rudolfb aDepartment of Biology, Louisiana State University, Baton Rouge, LA 70803; and bDepartment of BioSciences, Rice University, Houston, TX 77005 Edited by Rodolfo Dirzo, Stanford University, Stanford, CA, and approved May 12, 2016 (received for review October 16, 2015) Understanding how changes to the quality of habitat patches affect resource quality, weather, or predation risk) can carry over into new the distribution of species across the whole landscape is critical in our environments by altering the adult traits of individuals, including human-dominated world and changing climate. Although patterns of emigrants (16, 18). These environmentally induced effects operate species’ abundances across a landscape are clearly influenced by dis- through mechanisms, such as plasticity and body condition (18), and persal among habitats and local species interactions, little is known can alter many key life-history traits, including morphology, body size about how the identity and origin of dispersers affect these patterns. and allometry, diet, antipredator defenses, fecundity, or survival (19– Because traits of individuals are altered by experiences in their natal 27). Importantly, such carryover effects can alter individual traits habitat, differences in the natal habitat of dispersers can carry for a lifetime, and persist across multiple generations via maternal/ over when individuals disperse to new habitats and alter their parental effects (28, 29). Such persistent effects challenge the com- fitness and interactions with other species. We manipulated the mon assumption implicit in much theory that individuals simply presence or absence of such carried-over natal habitat effects for up to “reset” traits when dispersing. This assumption may be adequate in eight generations to examine their influence on two interacting species perfectly homogenous environments, because all individuals will across multiple dispersal rates and different habitat compositions. We have carried-over traits that “match” whichever habitat they found that experimentally accounting for the natal habitat of dispersers enter. However, in heterogeneous environments, dispersing indi- significantly influenced competitive outcomes at all spatial scales and viduals frequently encounter a habitat with conditions that differ increased total community biomass within a landscape. However, the from its natal habitat, and phenotypes of dispersing individuals will direction and magnitude of the impact of natal habitat effects was not “match” their current environment because of carryover effects ECOLOGY dependent upon landscape type and dispersal rate. Interestingly, ef- of their natal habitat conditions (30). This mismatch can alter fects of natal habitats increased the difference between species population dynamics (31–34) and interactions with other species performance across the landscape, suggesting that natal habitat (35). For example, snails with antipredator shell morphologies effects could alter competitive interactions to promote spatial coexis- from past predator experiences are vulnerable when they encounter tence. Given that heterogeneity in habitat quality is ubiquitous in nature, environments with new predator types (36). Alternatively, a resource- natal habitat effects are likely important drivers of spatial community rich natal environment for organisms from beetles (34) to birds structure and could promote variation in species performance, which (37) can result in “silver spoon effects” and increase the success may help facilitate spatial coexistence. The results have important impli- of individuals and populations in new environments, even if they cations for conservation and invasive species management. are low quality or mismatching habitats (18, 34, 37). Although increasing evidence suggest that carryover effects are both com- carryover effects | natal habitat effect | competition | metacommunity | mon and important for the structure of natural communities dispersal (15, 16, 35, 38, 39), their interactions with dispersal and variable habitats are not well studied (40). Consequently, how carryover ommunities do not exist in a vacuum; instead, they are effects influence species interactions and distributions across the Cconnected to each other through dispersal of interacting landscape is still poorly understood. species. Consequently, dispersal among different kinds of habitat patches is increasingly recognized as a key factor driving the Significance dynamics and structure of communities from local to regional spatial scales (1–5). In classic models, the persistence and dy- Communities do not exist in a vacuum; instead, they are connected namics of populations within a patch are determined by two fac- to each other through dispersal of interacting species. As a result, tors: the rate of dispersal between patches of habitat and the understanding how changes to the quality of habitat patches species fitness within each local patch (6–8). This view has per- affect communities across the whole landscape is critical in our sisted into metacommunity theory (multiple communities con- human-dominated world and changing climate. When individuals nected by dispersal of individuals between the patches of habitat disperse, they “carry” traits shaped by their natal environment to they occur in) as well, where the influence of dispersers on com- their destinations. Using replicated laboratory landscapes with munity dynamics is generally considered only in terms of their two competing species, we show that these historic effects of natal numbers (i.e., dispersal rate) and habitat-specific performance (1, – habitats have dramatic influences on community structure at all 9 11). Implicit in this case, and for most of spatial ecology, is that spatial scales and multiple dispersal rates. Such historic effects are the interactions and population dynamics within a habitat are ubiquitous in nature, suggesting that changes to local habitat quality solely determined by the quality of that habitat. However, this can have important effects on regional community structure. approach ignores the often substantial variation in individual traits and fitness within and across habitats in a natural system, which Author contributions: B.G.V. and V.H.W.R. designed research; B.G.V. performed research; could alter community dynamics and composition (12–15). B.G.V. analyzed data; and B.G.V. and V.H.W.R. wrote the paper. In metacommunities, one important source of individual varia- The authors declare no conflict of interest. tion arises from “carryover effects,” which can occur when early-life This article is a PNAS Direct Submission. (natal) experience affects later adult traits in a different time or Data deposition: The data reported in this paper have been deposited in the DRYAD place (16, 17). Carryover effects of natal habitat quality present an digital repository, datadryad.org (doi:10.5061/dryad.2gp80). interesting case of individual variation, as by definition their oc- 1To whom correspondence should be addressed. Email: [email protected]. currence is mediated by spatial variation and dispersal (16, 17). For This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. example, conditions experienced in the natal environment (e.g., 1073/pnas.1520536113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1520536113 PNAS Early Edition | 1of6 Downloaded by guest on October 2, 2021 35, 43). Furthermore, the offspring of beetles who developed in oat flour have prolonged development times and continue to exhibit higher cannibalism/pre- dation rates, indicating transgenerational effect of natal habitat quality (34). As a consequence, populations of both species founded by individuals from wheat flour grow faster to higher population sizes in either habitat, whereas individuals who come from oat are better competitors who are less likely to be excluded by the other species (34, 35). For additional details on how carryover effects alter both species behavior and performance, see refs. 34, 35, and 44. Experiment. To determine how carryover effects of natal habitat quality influence species distribution across different habitat patches, we factorially manipulated three factors: (i) frequency and spatial arrangement of patches with high- (wheat) vs. low- (oat) habitat quality (i.e., habitat heterogeneity) to create the potential for phenotype-environment mismatch, (ii) dispersal between these patches, and (iii) whether carryover effects matched the natal or new habitat of dispersing individuals. These treatments result in a 2 landscape (HLH and LHL) (Fig. 1) × 3 dispersal treatments (low, 5%, medium, 10%, and high, 40%, of individuals in − each patch emigrate to the adjacent patches month 1) × 2 carryover effects (phenotype matches natal vs. new habitat) factorial design for 12 total treatment groups (Fig. 1). Each landscape had three patches, each consisting of a 7-dram vial with 3.6 g of oat or wheat flour. The two landscape types differed in their con- figuration of oat (L, low-habitat quality) vs. wheat (H, high-habitat quality) hab- itat patch, representing a landscape where either patches with high (HLH) or low Fig. 1. Schematic of the experimental set-up of microcosm “landscapes.” (LHL) habitat quality were more frequent (Fig. 1). We replicated the 12 treatments There are two configurations (landscapes) of patches: