Carryover effects drive competitive dominance in spatially structured environments Benjamin G. Van Allena,b,1 and Volker H. W. Rudolfb a
Department 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)
carryover effects dispersal
| natal habitat effect | competition | metacommunity |
C
ommunities do not exist in a vacuum; instead, they are connected to each other through dispersal of interacting species. Consequently, dispersal among different kinds of habitat patches is increasingly recognized as a key factor driving the dynamics and structure of communities from local to regional spatial scales (1–5). In classic models, the persistence and dynamics of populations within a patch are determined by two factors: the rate of dispersal between patches of habitat and the species fitness within each local patch (6–8). This view has persisted into metacommunity theory (multiple communities connected by dispersal of individuals between the patches of habitat they occur in) as well, where the influence of dispersers on community dynamics is generally considered only in terms of their numbers (i.e., dispersal rate) and habitat-specific performance (1, 9–11). Implicit in this case, and for most of spatial ecology, is that the interactions and population dynamics within a habitat are solely determined by the quality of that habitat. However, this approach ignores the often substantial variation in individual traits and fitness within and across habitats in a natural system, which could alter community dynamics and composition (12–15). In metacommunities, one important source of individual variation arises from “carryover effects,” which can occur when early-life (natal) experience affects later adult traits in a different time or place (16, 17). Carryover effects of natal habitat quality present an interesting case of individual variation, as by definition their occurrence is mediated by spatial variation and dispersal (16, 17). For example, conditions experienced in the natal environment (e.g., www.pnas.org/cgi/doi/10.1073/pnas.1520536113
resource quality, weather, or predation risk) can carry over into new environments by altering the adult traits of individuals, including emigrants (16, 18). These environmentally induced effects operate through mechanisms, such as plasticity and body condition (18), and can alter many key life-history traits, including morphology, body size and allometry, diet, antipredator defenses, fecundity, or survival (19– 27). Importantly, such carryover effects can alter individual traits for a lifetime, and persist across multiple generations via maternal/ parental effects (28, 29). Such persistent effects challenge the common assumption implicit in much theory that individuals simply “reset” traits when dispersing. This assumption may be adequate in perfectly homogenous environments, because all individuals will have carried-over traits that “match” whichever habitat they enter. However, in heterogeneous environments, dispersing individuals frequently encounter a habitat with conditions that differ from its natal habitat, and phenotypes of dispersing individuals will not “match” their current environment because of carryover effects of their natal habitat conditions (30). This mismatch can alter population dynamics (31–34) and interactions with other species (35). For example, snails with antipredator shell morphologies from past predator experiences are vulnerable when they encounter environments with new predator types (36). Alternatively, a resourcerich natal environment for organisms from beetles (34) to birds (37) can result in “silver spoon effects” and increase the success of individuals and populations in new environments, even if they are low quality or mismatching habitats (18, 34, 37). Although increasing evidence suggest that carryover effects are both common and important for the structure of natural communities (15, 16, 35, 38, 39), their interactions with dispersal and variable habitats are not well studied (40). Consequently, how carryover effects influence species interactions and distributions across the landscape is still poorly understood. Significance Communities do not exist in a vacuum; instead, they are connected to each other through dispersal of interacting species. As a result, understanding how changes to the quality of habitat patches affect communities across the whole landscape is critical in our human-dominated world and changing climate. When individuals disperse, they “carry” traits shaped by their natal environment to their destinations. Using replicated laboratory landscapes with two competing species, we show that these historic effects of natal habitats have dramatic influences on community structure at all spatial scales and multiple dispersal rates. Such historic effects are ubiquitous in nature, suggesting that changes to local habitat quality can have important effects on regional community structure. Author contributions: B.G.V. and V.H.W.R. designed research; B.G.V. performed research; B.G.V. analyzed data; and B.G.V. and V.H.W.R. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. Data deposition: The data reported in this paper have been deposited in the DRYAD digital repository, datadryad.org (doi:10.5061/dryad.2gp80). 1
To whom correspondence should be addressed. Email: [email protected].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 1073/pnas.1520536113/-/DCSupplemental.
PNAS | June 21, 2016 | vol. 113 | no. 25 | 6939–6944
ECOLOGY
Understanding how changes to the quality of habitat patches affect the distribution of species across the whole landscape is critical in our human-dominated world and changing climate. Although patterns of species’ abundances across a landscape are clearly influenced by dispersal among habitats and local species interactions, little is known about how the identity and origin of dispersers affect these patterns. Because traits of individuals are altered by experiences in their natal habitat, differences in the natal habitat of dispersers can carry over when individuals disperse to new habitats and alter their fitness and interactions with other species. We manipulated the presence or absence of such carried-over natal habitat effects for up to eight generations to examine their influence on two interacting species across multiple dispersal rates and different habitat compositions. We found that experimentally accounting for the natal habitat of dispersers significantly influenced competitive outcomes at all spatial scales and increased total community biomass within a landscape. However, the direction and magnitude of the impact of natal habitat effects was dependent upon landscape type and dispersal rate. Interestingly, effects of natal habitats increased the difference between species performance across the landscape, suggesting that natal habitat effects could alter competitive interactions to promote spatial coexistence. Given that heterogeneity in habitat quality is ubiquitous in nature, natal habitat effects are likely important drivers of spatial community structure and could promote variation in species performance, which may help facilitate spatial coexistence. The results have important implications for conservation and invasive species management.
35, 43). Furthermore, the offspring of beetles who developed in oat flour have prolonged development times and continue to exhibit higher cannibalism/predation 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.
Fig. 1. Schematic of the experimental set-up of microcosm “landscapes.” There are two configurations (landscapes) of patches: HLH (high-, low-, then high-quality habitats) and LHL (low-, high-, then low-quality habitats). Tan patches indicate wheat flour/high-quality habitat and dark gray patches indicate oat flour/low-quality habitat. Beetles initially started in the patch labeled with their species name, then moved according to dispersal treatments (low = 5%, medium = 10%, and high = 40%) in the directions marked by the black arrows. To allow or prevent natal habitats from influencing the phenotypes of dispersing individuals, we replaced dispersing individuals from a habitat patch with individuals born in stock colonies with habitat types that either matched the natal habitat (i.e., phenotypes of dispersers are allowed be influenced by natal habitats) or matched the new habitat (i.e., no carryover effects of natal habitats). Colors of beetles indicate natal habitat-induced phenotypes (i.e., tan beetles developed in wheat flour and dark gray beetles in oat flour). With carryover effects, individuals moving from the microcosm HLH middle patch (for example) would be replaced with individuals born in the middle patch habitat type, oat flour in this case. Without carryover effects, the dispersing individuals would be replaced with individuals born in the destination habitat type, wheat flour in this case.
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 configuration of oat (L, low-habitat quality) vs. wheat (H, high-habitat quality) habitat patch, representing a landscape where either patches with high (HLH) or low (LHL) habitat quality were more frequent (Fig. 1). We replicated the 12 treatments 6 times for 72 independent sets of experimental landscapes with a total of 72 × 3 patches per landscape = 216 habitat patches. The six replications of the experimental design were divided into blocks with associated stock populations. For each block of treatments, we assigned eight stock populations, two oat and two wheat stock colonies per species (which were placed next to their experimental populations in that block), for a total of 48 stock colonies across the experiment. Stock colonies were maintained as standard laboratory stocks in 80 g of oat or wheat. Each block of landscapes with associated stock colonies was placed into one of three environmental chambers, which were kept at 30 °C (±1 °C) and 30% relative humidity (±5%). Details of our experimental methods and the initiation of the experiment can be found in SI Methods. Three
To identify how carryover effects influence the distribution of interacting species across landscapes with variable habitats, we experimentally manipulated: (i) phenotypes of dispersing individuals to match their natal or new environment, (ii) dispersal rates, and (iii) habitat composition across three habitat patch “landscapes” for two competing flour beetles. We specifically focused on how the presence or absence of natal habitat effects in dispersing individuals carried over to alter competitive dominance, relative abundance, and total abundance of both species at local (patch) and landscape scales. Methods Study Species. We tested how carryover effects influenced the distribution of competing species across multiple habitats using laboratory microcosm “landscapes” populated by two competing species of flour beetle, Tribolium castaneum and Tribolium confusum. The entire life cycle of a flour beetle can take place in milled grain, although beetles can eat many small or soft food items, such as small animal prey, including their own young and the young of other Tribolium species (41). These two species therefore compete largely through intraguild predation in maintained environments (42). The flour type in which beetles develop determines the phenotype of adults, leading to long-lasting habitat-mediated carryover effects. Oat media is a relatively low-quality (nutrient poor) habitat (LHL, low-, high-, then low-quality habitats) for both beetle species, whereas wheat media is the standard high-quality habitat (HLH, high-, low-, then high-quality habitats) for both species. Development in oat flour reduces adult body size, alters adult lifespan, reduces fecundity, and increases cannibalism/predation rates relative to development in wheat flour (34, 35). Although both species are influenced by the flour type in which they develop, T. castaneum is more negatively affected by low-quality (oat) habitat, but performs better in high-quality (wheat) habitat than T. confusum (34,
6940 | www.pnas.org/cgi/doi/10.1073/pnas.1520536113
Fig. 2. Mean abundance (±1 SEM) of T. castaneum (red lines), T. confusum (blue lines), and the total of both species abundance (black lines) with or without carryover effects of natal habitats in immigrants across landscape configurations with more low-quality habitat, LHL (A–C) and more high-quality habitat, HLH (D–G) and different dispersal-rate treatments (i.e., proportion of dispersing individuals: low = 5%, mid = 10%, high = 40%). n = 69.
Van Allen and Rudolf
Factor Natal habitat effects (Y/N) Dispersal rate Landscape configuration (HLH or LHL) Landscape × Dispersal Natal habitat × Landscape Natal habitat × Dispersal Natal habitat × Landscape × Dispersal Random effect of block: P > 0.05
χ2
P
7.59 36.92 252.74 20.84 0.29 1.93 3.49
0.006
Department 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)
carryover effects dispersal
| natal habitat effect | competition | metacommunity |
C
ommunities do not exist in a vacuum; instead, they are connected to each other through dispersal of interacting species. Consequently, dispersal among different kinds of habitat patches is increasingly recognized as a key factor driving the dynamics and structure of communities from local to regional spatial scales (1–5). In classic models, the persistence and dynamics of populations within a patch are determined by two factors: the rate of dispersal between patches of habitat and the species fitness within each local patch (6–8). This view has persisted into metacommunity theory (multiple communities connected by dispersal of individuals between the patches of habitat they occur in) as well, where the influence of dispersers on community dynamics is generally considered only in terms of their numbers (i.e., dispersal rate) and habitat-specific performance (1, 9–11). Implicit in this case, and for most of spatial ecology, is that the interactions and population dynamics within a habitat are solely determined by the quality of that habitat. However, this approach ignores the often substantial variation in individual traits and fitness within and across habitats in a natural system, which could alter community dynamics and composition (12–15). In metacommunities, one important source of individual variation arises from “carryover effects,” which can occur when early-life (natal) experience affects later adult traits in a different time or place (16, 17). Carryover effects of natal habitat quality present an interesting case of individual variation, as by definition their occurrence is mediated by spatial variation and dispersal (16, 17). For example, conditions experienced in the natal environment (e.g., www.pnas.org/cgi/doi/10.1073/pnas.1520536113
resource quality, weather, or predation risk) can carry over into new environments by altering the adult traits of individuals, including emigrants (16, 18). These environmentally induced effects operate through mechanisms, such as plasticity and body condition (18), and can alter many key life-history traits, including morphology, body size and allometry, diet, antipredator defenses, fecundity, or survival (19– 27). Importantly, such carryover effects can alter individual traits for a lifetime, and persist across multiple generations via maternal/ parental effects (28, 29). Such persistent effects challenge the common assumption implicit in much theory that individuals simply “reset” traits when dispersing. This assumption may be adequate in perfectly homogenous environments, because all individuals will have carried-over traits that “match” whichever habitat they enter. However, in heterogeneous environments, dispersing individuals frequently encounter a habitat with conditions that differ from its natal habitat, and phenotypes of dispersing individuals will not “match” their current environment because of carryover effects of their natal habitat conditions (30). This mismatch can alter population dynamics (31–34) and interactions with other species (35). For example, snails with antipredator shell morphologies from past predator experiences are vulnerable when they encounter environments with new predator types (36). Alternatively, a resourcerich natal environment for organisms from beetles (34) to birds (37) can result in “silver spoon effects” and increase the success of individuals and populations in new environments, even if they are low quality or mismatching habitats (18, 34, 37). Although increasing evidence suggest that carryover effects are both common and important for the structure of natural communities (15, 16, 35, 38, 39), their interactions with dispersal and variable habitats are not well studied (40). Consequently, how carryover effects influence species interactions and distributions across the landscape is still poorly understood. Significance Communities do not exist in a vacuum; instead, they are connected to each other through dispersal of interacting species. As a result, understanding how changes to the quality of habitat patches affect communities across the whole landscape is critical in our human-dominated world and changing climate. When individuals disperse, they “carry” traits shaped by their natal environment to their destinations. Using replicated laboratory landscapes with two competing species, we show that these historic effects of natal habitats have dramatic influences on community structure at all spatial scales and multiple dispersal rates. Such historic effects are ubiquitous in nature, suggesting that changes to local habitat quality can have important effects on regional community structure. Author contributions: B.G.V. and V.H.W.R. designed research; B.G.V. performed research; B.G.V. analyzed data; and B.G.V. and V.H.W.R. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. Data deposition: The data reported in this paper have been deposited in the DRYAD digital repository, datadryad.org (doi:10.5061/dryad.2gp80). 1
To whom correspondence should be addressed. Email: [email protected].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 1073/pnas.1520536113/-/DCSupplemental.
PNAS | June 21, 2016 | vol. 113 | no. 25 | 6939–6944
ECOLOGY
Understanding how changes to the quality of habitat patches affect the distribution of species across the whole landscape is critical in our human-dominated world and changing climate. Although patterns of species’ abundances across a landscape are clearly influenced by dispersal among habitats and local species interactions, little is known about how the identity and origin of dispersers affect these patterns. Because traits of individuals are altered by experiences in their natal habitat, differences in the natal habitat of dispersers can carry over when individuals disperse to new habitats and alter their fitness and interactions with other species. We manipulated the presence or absence of such carried-over natal habitat effects for up to eight generations to examine their influence on two interacting species across multiple dispersal rates and different habitat compositions. We found that experimentally accounting for the natal habitat of dispersers significantly influenced competitive outcomes at all spatial scales and increased total community biomass within a landscape. However, the direction and magnitude of the impact of natal habitat effects was dependent upon landscape type and dispersal rate. Interestingly, effects of natal habitats increased the difference between species performance across the landscape, suggesting that natal habitat effects could alter competitive interactions to promote spatial coexistence. Given that heterogeneity in habitat quality is ubiquitous in nature, natal habitat effects are likely important drivers of spatial community structure and could promote variation in species performance, which may help facilitate spatial coexistence. The results have important implications for conservation and invasive species management.
35, 43). Furthermore, the offspring of beetles who developed in oat flour have prolonged development times and continue to exhibit higher cannibalism/predation 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.
Fig. 1. Schematic of the experimental set-up of microcosm “landscapes.” There are two configurations (landscapes) of patches: HLH (high-, low-, then high-quality habitats) and LHL (low-, high-, then low-quality habitats). Tan patches indicate wheat flour/high-quality habitat and dark gray patches indicate oat flour/low-quality habitat. Beetles initially started in the patch labeled with their species name, then moved according to dispersal treatments (low = 5%, medium = 10%, and high = 40%) in the directions marked by the black arrows. To allow or prevent natal habitats from influencing the phenotypes of dispersing individuals, we replaced dispersing individuals from a habitat patch with individuals born in stock colonies with habitat types that either matched the natal habitat (i.e., phenotypes of dispersers are allowed be influenced by natal habitats) or matched the new habitat (i.e., no carryover effects of natal habitats). Colors of beetles indicate natal habitat-induced phenotypes (i.e., tan beetles developed in wheat flour and dark gray beetles in oat flour). With carryover effects, individuals moving from the microcosm HLH middle patch (for example) would be replaced with individuals born in the middle patch habitat type, oat flour in this case. Without carryover effects, the dispersing individuals would be replaced with individuals born in the destination habitat type, wheat flour in this case.
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 configuration of oat (L, low-habitat quality) vs. wheat (H, high-habitat quality) habitat patch, representing a landscape where either patches with high (HLH) or low (LHL) habitat quality were more frequent (Fig. 1). We replicated the 12 treatments 6 times for 72 independent sets of experimental landscapes with a total of 72 × 3 patches per landscape = 216 habitat patches. The six replications of the experimental design were divided into blocks with associated stock populations. For each block of treatments, we assigned eight stock populations, two oat and two wheat stock colonies per species (which were placed next to their experimental populations in that block), for a total of 48 stock colonies across the experiment. Stock colonies were maintained as standard laboratory stocks in 80 g of oat or wheat. Each block of landscapes with associated stock colonies was placed into one of three environmental chambers, which were kept at 30 °C (±1 °C) and 30% relative humidity (±5%). Details of our experimental methods and the initiation of the experiment can be found in SI Methods. Three
To identify how carryover effects influence the distribution of interacting species across landscapes with variable habitats, we experimentally manipulated: (i) phenotypes of dispersing individuals to match their natal or new environment, (ii) dispersal rates, and (iii) habitat composition across three habitat patch “landscapes” for two competing flour beetles. We specifically focused on how the presence or absence of natal habitat effects in dispersing individuals carried over to alter competitive dominance, relative abundance, and total abundance of both species at local (patch) and landscape scales. Methods Study Species. We tested how carryover effects influenced the distribution of competing species across multiple habitats using laboratory microcosm “landscapes” populated by two competing species of flour beetle, Tribolium castaneum and Tribolium confusum. The entire life cycle of a flour beetle can take place in milled grain, although beetles can eat many small or soft food items, such as small animal prey, including their own young and the young of other Tribolium species (41). These two species therefore compete largely through intraguild predation in maintained environments (42). The flour type in which beetles develop determines the phenotype of adults, leading to long-lasting habitat-mediated carryover effects. Oat media is a relatively low-quality (nutrient poor) habitat (LHL, low-, high-, then low-quality habitats) for both beetle species, whereas wheat media is the standard high-quality habitat (HLH, high-, low-, then high-quality habitats) for both species. Development in oat flour reduces adult body size, alters adult lifespan, reduces fecundity, and increases cannibalism/predation rates relative to development in wheat flour (34, 35). Although both species are influenced by the flour type in which they develop, T. castaneum is more negatively affected by low-quality (oat) habitat, but performs better in high-quality (wheat) habitat than T. confusum (34,
6940 | www.pnas.org/cgi/doi/10.1073/pnas.1520536113
Fig. 2. Mean abundance (±1 SEM) of T. castaneum (red lines), T. confusum (blue lines), and the total of both species abundance (black lines) with or without carryover effects of natal habitats in immigrants across landscape configurations with more low-quality habitat, LHL (A–C) and more high-quality habitat, HLH (D–G) and different dispersal-rate treatments (i.e., proportion of dispersing individuals: low = 5%, mid = 10%, high = 40%). n = 69.
Van Allen and Rudolf
Factor Natal habitat effects (Y/N) Dispersal rate Landscape configuration (HLH or LHL) Landscape × Dispersal Natal habitat × Landscape Natal habitat × Dispersal Natal habitat × Landscape × Dispersal Random effect of block: P > 0.05
χ2
P
7.59 36.92 252.74 20.84 0.29 1.93 3.49
0.006
