Contemporary natural populations are faced with an unprecedented array of challenges as a direct result of anthropogenic influences on the environment. These anthropogenic influences may lead to environmental alterations that exceed the rate of change contemporary natural populations have historically experienced. Rapidly changing environmental conditions place natural populations at risk of extinction, and the current rate of extinction is increasing [1, 2]. When rapid environmental change occurs, the likelihood of population persistence can be enhanced through a number of mechanisms including dispersal , phenotypic plasticity , and genetic adaptation . Thus, understanding the dynamics of adaptive responses to changing environments is of central importance to evolutionary biologists, ecologists, and conservation biologists.
One of the most ubiquitous anthropogenic influences on ecosystems is the introduction of non-native species. The evolutionary component of species invasions has been the growing focus of studies on the adaptation of introduced species in a novel environment and the evolutionary consequences for native species in invaded communities [6, 7]. Intentional and accidental introductions of non-native species into naive communities in many cases comprise a particularly dramatic environmental change that can result in rapid adaptive change [5, 8]. While most examples of rapid adaptation stem from the ecological and evolutionary response of invaders in novel environments , native species within an invaded habitat frequently exhibit adaptive responses to introductions of novel species [9–12]. In special cases where the introduced species is a novel predator, native prey species can experience abrupt changes in the intensity or direction of natural selection [5, 13]. In order to persist during changes in the selective environment, native prey populations require rapid evolution of behaviour, morphology, or life-history traits . Examples of specific consequences of altered selection regimes arising from introduced predators include the acquisition of alarm responses , changes in patterns of diel vertical migration patterns , altered habitat use , increased escape ability , and reductions in body size and age at maturity .
Planktivorous fish are commonly introduced into freshwater systems for recreational fishing purposes [19–21] and can pose particularly strong selective challenges for native planktonic invertebrate populations. Many fish species, including salmonids, are highly efficient visual predators that selectively feed upon larger, more conspicuous zooplankton [22–25]. A primary prey item for fish, Daphnia, are especially vulnerable to fish predation due to their relatively large body sizes and poor swimming abilities . However, Daphnia are capable of rapid evolutionary response to changing environmental conditions [27, 28], and they have long been used as a model ecological system to study the consequences of changing selective challenges arising from fish introductions [29–32]. Novel size-selective predation on native Daphnia populations has precipitated rapid evolution in traits primarily related to detection avoidance, including alterations in patterns of diel vertical migration (DVM) [16, 33] and reduced body size [23, 30, 32]. Fish predation can also result in changes in life-history traits, such as clutch size and growth rate .
The alpine lakes throughout the Sierra Nevada in eastern California, USA are ideally suited for investigation of the process of rapid adaptive evolution in response to abrupt changes in the selective environment. The lakes of the Sierra Nevada have been the subjects of extensive ecological study [35–37] in large part because the history of fish introductions is well documented. Nearly all lakes in the Sierra Nevada were historically fishless but the majority were stocked with one or more species of trout during the past century [36, 37]. Fish presence/absence is often the best predictor of zooplankton species composition (e.g., when fish are present in a lake, larger zooplankton are usually absent ), and the introduction of non-native fish into many historically fishless lakes has led to the extirpation of vulnerable invertebrate species [35–37].
The Daphnia community in alpine lakes of the Sierra Nevada is characterized by a single large-bodied, highly pigmented species, Daphnia melanica (genetic analyses indicate that the Daphnia middendorffiana referenced in earlier papers [35–39] is actually D. melanica; M. Pfrender, unpublished data). Because of its large body size (up to 4 mm) and dark pigmentation, this conspicuous species is particularly vulnerable to introduced fish predators. However, in a subset of lakes non-native fish and Daphnia coexist , providing a unique opportunity to study the evolutionary consequences of introduced fish predators.
This study reports the phenotypic patterns and rates of divergence in naturally occurring populations of D. melanica coexisting with introduced fish predators. Several studies have reported rapid adaptive changes in native prey populations following the introduction of novel predators. However, few studies report estimates of the rate of adaptation or divergence in conjunction with observed patterns. Quantitative estimates of evolutionary rates facilitate comparisons across studies, traits, taxa, and time frames . Because we estimate rates of divergence in prey populations exposed to novel predators, we discuss our results in the context of other studies that have examined patterns of divergence, as well as those studies in which evolutionary rates were estimated.