(a) Effects of invasion, evolution and coevolution
Ecologists have traditionally focused on functional diversity at or above the species level to explain community and ecosystem patterns and processes (Hooper et al. 2005
). For this reason, species introductions and invasions have garnered much attention. Invading species introduce new phenotypes into communities, thereby initiating novel ecological interactions and modifying existing ones (White et al. 2006
). However, phenotype distributions and ecological interactions can also change as a result of evolutionary and coevolutionary processes including those occurring over contemporary (ecological) time scales (Thompson 1999
; Hairston et al. 2005
). We examined the effects of guppy evolution and Rivulus
–guppy coevolution on model Trinidadian stream ecosystems and compared these effects with the effects of guppy invasion. Our results show that the magnitude of evolutionary and coevolutionary effects can exceed those of traditional ecological effects.
Guppies and Rivulus show substantial interspecific differences in body size, excretion rates and trophic interactions. Owing to body size differences, guppies drove higher nutrient excretion rates than did Rivulus. In addition, guppies consume epilithic algae, whereas Rivulus do not. Due to these interspecific differences, guppy invasion might be expected to have important impacts on ecosystem properties. However, our results show that guppy invasion (the substitution of half the biomass of Rivulus for an equal biomass of guppies) did not drastically alter algal dynamics, invertebrate biomass or decomposition rates (a and ). The lack of a significant effect of guppy invasion on algae may be due to the opposing forces of nutrient excretion and algal consumption. Algal standing stocks represent primary production minus consumption. Guppy invasion caused a significant increase in N-excretion and a marginally significant increase in P-excretion (), which are expected to increase primary production. However, algae consumption by guppies may have offset any increases in primary production, resulting in no net change in algal biomass or accrual rates. We observed a small increase in aquatic invertebrate biomass caused by guppy invasion, but the effect was not significant (a and ). This lack of a significant effect may have been due to either substantial invertebrate consumption by guppies and/or compensatory feeding by Rivulus when released (somewhat) from intraspecific competition.
Guppy populations display substantial intraspecific variation in life-history traits and morphology as a result of local adaptation to different predation regimes. HP guppies drove significantly higher rates of N-excretion compared with LP guppies (), perhaps as a consequence of life-history evolution on fish community body size structure. LP guppies consumed greater quantities of algae compared with HP guppies (), perhaps due to differences in morphology and foraging behaviour. Owing to these differences, guppy evolution might be expected to have important effects on ecosystem properties. Our results show that guppy evolution did indeed have a significant influence on algal biomass and accrual rates, with HP guppies driving increases in algae relative to LP guppies (b and ).
Why did guppy evolution cause significant changes in algal biomass and accrual rates while guppy invasion did not? For guppy invasion, the effects of nutrient excretion and algal consumption appeared to work in opposite directions on algal biomass. However, for guppy evolution, these factors appeared to work in concert. Compared with LP guppies, HP guppies excreted N at higher rates, increasing primary production, and fed on algae at lower rates, decreasing algal consumption. Both effects served to increase algal standing stocks, and the net result was a significant increase in algal biomass and accrual rates for mesocosms containing HP guppies (b and ).
Interestingly, guppy populations from both HP and LP localities showed consistent sex differences in algal consumption, with males of both types consuming more algae than females (). Previous studies have suggested that male and female guppies show different patterns of morphological divergence across predation regimes and other habitat features (Hendry et al. 2006
) and show different degrees of phenotypic plasticity when faced with alternative food presentations (Robinson & Wilson 1995
). One possible explanation for sex-specific aspects of phenotypic divergence and plasticity in trophic morphology is the link between algae consumption and male guppy colour patterns, which are important as mating cues and respond to the quantity of algae-derived carotenoids in the diet (Grether 2000
; Grether et al. 2005
In streams where Rivulus
and guppies coexist in the absence of other fish species, predation and competition may drive coevolution between these species. We found that the coevolved Rivulus
–guppy treatment had a lower biomass of aquatic invertebrates than the non-coevolved treatments (figure 1c
and 4). The reduction of a shared prey resource in the coevolved treatment suggests that competition between guppies and Rivulus
may have selected for niche convergence (Scheffer & van Nes 2006
) and enhanced competitive ability (Hairston 1980
). If coevolved guppies and Rivulus
can more efficiently exploit aquatic invertebrates, this hypothesis could explain why coevolution significantly decreased invertebrate biomass. Behavioural observations conducted in the mesocosms provide some support for this interpretation. Guppies and Rivulus
showed less habitat segregation and interspecific avoidance behaviour in the coevolved treatment than in the non-coevolved treatments (B. A. Lamphere 2007, unpublished data). However, further work is needed to test this hypothesized mechanism.
The current paradigm for predicting ecological function is based primarily on overall phenotypic similarity or phylogenetic relatedness—the more dissimilar or distantly related two forms, the more probable they will be functionally distinct (Webb et al. 2002
; Hooper et al. 2005
). This assumption underlies the use of species as functional units, as overall phenotypic differences found among species are generally larger than differences within species. Based on this assumption, one would predict that the relative effect sizes in our experiment would be: guppy invasion>guppy evolution>Rivulus
–guppy coevolution. However, our results did not generally conform to this pattern (). The effect of guppy evolution was greater than the effect of guppy invasion for algal biomass, algal accrual rates, invertebrate biomass and decomposition rates. The effect of Rivulus
–guppy coevolution was greater than the effect of guppy invasion for invertebrate biomass and decomposition rates. These results suggest that phenotypic dissimilarity and phylogenetic relatedness are not always reliable predictors of ecological function. Given that contemporary evolution is prevalent in many species (Kinnison & Hendry 2001
), including those examined in this study, our findings also suggest that ongoing evolution may merit greater consideration in both basic and applied ecology.
The results of our experiment show that coevolution may be an important factor shaping ecosystem processes. The existence of coevolutionary effects in ecosystems is not unexpected. Ecological processes are often determined not by the phenotypic traits of one species (although the traits of some species may have inordinately large effects; Post & Palkovacs 2009
), but by how traits mediate interactions among many species (Urban & Skelly 2006
). What is unexpected about our results is the magnitude of coevolutionary effects. For invertebrate biomass and decomposition rates, the effect of coevolution was larger than the effects of either invasion or evolution ().
Interestingly, our results suggest that it is the source of invading guppies, rather than the invasion of guppies per se
, which determines algal biomass and accrual rates, key ecosystem properties. Relative to the RO condition, HP and LP guppy invasions had opposite effects on algal biomass and accrual rates. Perhaps equally intriguing, Rivulus
–guppy coevolution returned algal biomass and accrual rates to levels similar to their pre-guppy states. This finding suggests a note of caution for non-experimental studies of invasion. If we were to have compared algal biomass and accrual rates in natural streams at the eco-evolutionary equilibrium states that occur in nature (RO and coevolved Rivulus
–guppy), we may have concluded that the addition of guppies to the ecosystem has no significant effects. This scenario provides a potential example of how evolutionary processes may mask ecological dynamics (Yoshida et al. 2007
), an area of research that certainly warrants further investigation.
(b) Eco-evolutionary feedbacks
In this study, we examined the ecological effects of phenotypic divergence—the approach commonly used in community and ecosystem genetics (Whitham et al
; Johnson & Stinchcombe 2007
). We are able to draw inferences about the effects of evolution on ecosystem dynamics because previous research has shown that the phenotypes we examined are heritable and subject to contemporary evolution. However, it remains a frontier to experimentally examine the ecosystem effects of dynamically evolving (and coevolving) populations in the wild. Our results suggest that the ecosystem consequences of species invasions may derive, in part, from post-invasion evolution to new environmental conditions and that coevolution with other community members may contribute to community and ecosystem resilience. However, one potentially critical element that can only be entirely captured using dynamic experiments is the eco-evolutionary feedback (Fussmann et al. 2007
; Post & Palkovacs 2009
Eco-evolutionary feedbacks occur when organisms change the biotic or abiotic conditions of their environment and those changes then influence the direction of evolution (Laland et al. 1999
; Palkovacs & Post 2008
; Post & Palkovacs 2009
). Such feedbacks can change the ecological and evolutionary trajectories of systems, causing them to deviate from expectations based on fixed phenotype experiments (Habets et al. 2006
). We did not directly test eco-evolutionary feedbacks in this experiment, but we can use the results to speculate about potential feedback mechanisms. As revealed by previous studies, guppies from HP habitats typically experience greater resource availability due to increased algal standing stocks than do guppies from LP habitats (Grether et al. 2001
; Reznick et al. 2001
). The availability of algal resources appears to contribute to the evolution of female growth rates (Arendt & Reznick 2005
) and can influence the evolution of male guppy colour patterns (Grether 2000
; Grether et al. 2005
). Increases in algal biomass associated with HP environments have previously been interpreted as extrinsically determined features of the ecosystem—features to which guppies respond evolutionarily. By contrast, our findings suggest that guppy populations can influence algal availability as a by-product of the evolution of life-history traits, body size differences, morphological traits and dietary preferences. The scope for guppies to shape their ecosystem in natural streams is currently unknown. However, the experiment reported here raises the real possibility that previously documented evolutionary responses to increased algal availability may represent (at least in part) eco-evolutionary feedbacks. To examine this possibility, we have recently undertaken a series of dynamic experiments tracking the eco-evolutionary consequences of guppy invasion, guppy evolution and Rivulus
–guppy coevolution as they unfold in the wild.
Humans are a long-recognized global driver of species invasions. Therefore, conservation biologists focus much attention on the ecology of species invasions and on developing policies to slow the rate of species introductions. Only relatively recently has it been recognized that humans are also a global driver of intraspecific phenotypic change (Palumbi 2001
; Hendry et al. 2008
). Eco-evolutionary dynamics—the effects of ecology on contemporary evolution and the reciprocal effects of evolution (and coevolution) on ecological processes—provide a new framework to understand natural systems. However, broader integration of eco-evolutionary dynamics into applied ecology and conservation biology will probably depend upon additional studies similar to ours that provide empirical insights into the relative importance of evolution and coevolution in areas of conservation concern, such as species invasions, over-harvesting, habitat alteration and global climate change.