Rapid evolution in response to introduced predators I: rates and patterns of morphological and life-history trait divergence
© Fisk et al; licensee BioMed Central Ltd. 2007
Received: 09 September 2006
Accepted: 14 February 2007
Published: 14 February 2007
Introduced species can have profound effects on native species, communities, and ecosystems, and have caused extinctions or declines in native species globally. We examined the evolutionary response of native zooplankton populations to the introduction of non-native salmonids in alpine lakes in the Sierra Nevada of California, USA. We compared morphological and life-history traits in populations of Daphnia with a known history of introduced salmonids and populations that have no history of salmonid introductions.
Our results show that Daphnia populations co-existing with fish have undergone rapid adaptive reductions in body size and in the timing of reproduction. Size-related traits decreased by up to 13 percent in response to introduced fish. Rates of evolutionary change are as high as 4,238 darwins (0.036 haldanes).
Species introductions into aquatic habitats can dramatically alter the selective environment of native species leading to a rapid evolutionary response. Knowledge of the rates and limits of adaptation is an important component of understanding the long-term effects of alterations in the species composition of communities. We discuss the evolutionary consequences of species introductions and compare the rate of evolution observed in the Sierra Nevada Daphnia to published estimates of evolutionary change in ecological timescales.
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.
Patterns of divergence
Effects of introduced fish on morphological and life-history traits.
Patterns of character change
Summary of the results of linear regressions of trait values versus years with introduced fish.
Rates of divergence
Divergence rates in response to fish introductions.
Exposure Time (yrs)
Species introductions can precipitate rapid evolutionary responses in native species [12, 41, 42]. Several criteria have been proposed to identify cases of rapid adaptive evolution . Among the most important criteria are directional selection with a known cause, an additive genetic basis for traits under selection, and that the response to selection is likely adaptive. We believe our study adequately addresses all of these elements. First, size-selective predation by fish imposes strong directional selection on populations of Daphnia [16, 22, 23, 43], and in Sierra Nevada lakes the most conspicuous change in the selective environment is the recent introduction of salmonid fishes. Second, because we utilized a common garden experimental design, observed differences among our populations are genetic in nature. Furthermore, traits under selection in this study are known to show significant heritabilities in other species of Daphnia [44, 45] and often have substantial levels of additive genetic variation . Finally, the phenotypic response to directional selection is likely to be adaptive because changes we observed are consistent with expectations for populations under size-selective predation. Also useful in identifying rapid evolution is knowledge of the time scale in which the change has taken place and measures of character states before and after the selection event. Because the history of fish introductions is well documented in the Sierra Nevada we know the date of the initial fish stocking in our experimental lakes and the duration of exposure to altered predation regimes. Since this study is cross-sectional and not a temporal series we do not know with certainty what the Daphnia phenotypic states in the fish lakes were prior to fish introductions and subsequent selection. However, given that the three fishless lakes we examined did not differ from one another phenotypically, our assumption that phenotypic trait values from populations that have never been exposed to introduced salmonids are representative of trait values in populations prior to fish introductions is justified.
Our results show that introductions of novel fish predators are associated with a specific pattern of phenotypic change in Daphnia populations from alpine lakes in the Sierra Nevada. In comparison to historically fishless lakes, D. melanica that co-occur with introduced fish are smaller, have smaller offspring, reach maturity earlier and have shorter adult instar durations. Our results are in agreement with other studies showing that the introduction of non-native fish into fishless habitats produces a predictable pattern of rapid divergence from populations not containing fish (e.g., ).
The reduced body size observed in D. melanica populations that co-occur with introduced salmonids is consistent with other empirical observations of zooplankton responses to size-selective vertebrate predation. At the community level, size-selective predation by fish results in a shift in species composition such that smaller bodied species become numerically abundant. This shift in species composition can lead to a decrease in maximum zooplankton body length in as little as 20 years . Furthermore, examination of trout stomach contents show they not only contain a higher proportion of larger-bodied zooplankton species within a lake, but that trout preferentially feed upon genotypes conferring relatively larger body sizes within populations of vulnerable species. The effect of size selective fish predation within a population can manifest over quite short periods of time. For example, mean body size decreased when Daphnia were exposed to fish predation for only 50 days .
In addition to changes in body size, introductions of fish into naive Daphnia populations of the Sierra Nevada also resulted in changes in life-history strategies. Populations exposed to fish predation mature earlier and had fewer, smaller offspring in each clutch than populations from fishless lakes. The changes in clutch size and timing of reproduction are not surprising since these traits frequently co-vary with body size in Daphnia . Smaller Daphnia tend to carry fewer and/or smaller offspring [47–49].
Our estimates of divergence rates for body size and timing of reproduction are several times to an order of magnitude lower than those obtained in a comparable study of the evolutionary response of Trinidad guppies to introduced fish predators . One explanation for the lower observed rates is that much of the evolution in these populations occurred shortly after fish introductions, resulting in overestimates of the actual time during which evolution actually took place. The possibility of protracted sampling would then result in underestimates of the actual rate of phenotypic change. A second possibility for this observation is that the strength of selection in the Sierra Nevada Daphnia populations is not as intense as in the Trinidad guppy system. There are also a number of features of the biology of Daphnia that may contribute to a slower response to selection. Since Daphnia in these populations hatch from an "egg bank"  of diapausing eggs in lake bottom sediments there is a continual input of genotypes from earlier time periods. Genotypes from these earlier time periods may have never been exposed to the novel selective regime or had genotypic values that had not advanced as far in response to selection. The effect of this temporal mixing of genotypes would be to retard the realized rate of evolution . In addition, our estimates of the rate of adaptation is based on the simplifying assumption that one calendar year is equal to one generation. For temporary pond populations of Daphnia this is a reasonable assumption since these populations typically engage in a bout of sexual reproduction every year. However, for permanent lake-dwelling populations of Daphnia the reproductive cycle can be more complicated. Lake-dwelling populations may engage in sexual reproduction at highly irregular intervals with clones persisting for long periods of time via asexual reproduction. If the Sierra Nevada populations have engaged in sexual reproduction less frequently than on a yearly cycle our estimated rates would be lower than the actual per generation rates. Alternation of asexual and sexual reproduction may also influence the response to selection in two additional ways. First, a cyclic parthenogenetic mode of reproduction can induce oscillations of expressed genetic variation with low levels of expressed variation during periods of prolonged asexual reproduction punctuated by periods of enhanced expressed genetic variation immediately following a bout of sex . During periods of reduced expressed genetic variation populations would respond to phenotypic selection slowly. Second, the response to selection during periods of asexual reproduction can induce substantial gametic phase disequilibria (GPD; non-independence of allele identities at two or more loci). Sexual reproduction and recombination erodes GPD and, assuming an additive genetic basis to the trait, causes a shift in the mean phenotype in the opposite direction from that promoted by selection. This phenomenon is often referred to as genetic slippage and has been observed in a number of populations of Daphnia [28, 53, 54].
Previous work in the Sierra Nevada has shown that introduced fish have caused many Daphnia populations to go locally extinct [36–38]. Our study shows that extant Daphnia populations subjected to size-selective fish predation have divergent life-history and morphology compared to populations without fish. The divergence in lakes containing fish and Daphnia is in a direction consistent with adaptive evolution and occurred in less than 100 years. This study suggests that native species in aquatic systems are qualitatively similar to terrestrial species in their ability to respond through evolutionary change [43, 44]. In light of our results we suggest the rate of evolutionary response and limits to the degree of response will be important determinants of persistence of native populations when faced with selective challenges arising from species introductions, and over the long-term will have a profound influence on community structure.
Daphnia melanica used in this study were collected from seven permanent lakes in the central Sierra Nevada (Fig. 3). These lakes are located in the Humphreys, French Canyon, Upper Mono Creek, and Vogelsang basins at elevations ranging from 3150–3632 meters. Lakes sampled were chosen based on the results of zooplankton sampling [37, 38]. Three of these lakes have no history of salmonid introductions (referred to as "Fishless" populations): "Snowpole" (UTM Zone 11: 350430 E, 4123368 N); "Frog" (UTM Zone 11: 351079 E, 4124432 N); and Middle Skelton (UTM Zone 11: 298120 E, 4201298 N). The remaining four lakes have a known history of salmonid introductions including rainbow trout (Oncorhynchus mykiss), goldent trout (O. m., aguabonita), brown trout (Salmo trutta), and brook trout (Salvelinus fontinalis) and contain resident populations of Daphnia (referred to as "Fish" populations): Lower Goethe (UTM Zone 11: 349094 E, 4121242 N; fish first introduced in 1953); Puppet (UTM Zone 11: 346277 E, 4127817 N); Golden (UTM Zone 11: 343870 E, 4146114 N); and Evelyn (UTM Zone 11: 295393 E, 4186659 N). Based on California Dept. of Fish and Game unpublished stocking records, Lower Goethe Lake has been stocked with golden trout every other year since 1953. Puppet Lake has been stocked with golden trout every other year since 1951. Golden Lake was first stocked with golden trout in 1931 and restocked every other year until 1996. The resident golden trout population is self-sustaining. Evelyn Lake was initially stocked with brown trout in 1913. Brook trout were introduced in 1928, 1946, 1947, 1949, 1951, 1954 and 1958, and rainbow trout were introduced in 1939, 1942, 1944, 1957, 1962, and 1966. No stocking has occurred since 1966, and the resident rainbow trout population is self-sustaining.
Daphnia were collected from the study lakes using a 30 cm conical tow net and transported to the laboratory where they were maintained at 4°C for a period of 1–2 weeks. To maximize the amount of genetic variation captured from each population, mature females from the original field collections were then isolated and placed singly in 250 mL beakers containing 200 mL of filtered well-water. Since field collected individuals often carry asexually produced clutches in their brood pouch, this procedure ensured that no isolates were genotypically identical individuals released during the period from collection in the field until isolation in the lab. At 4°C, asexual offspring released prior to isolation in the lab would not have sufficient time to reach maturity. Stock cultures were established from these isolated individuals by clonal reproduction under constant conditions of temperature (15°C) and photoperiod (16L:8D). Daphnia were fed a vitamin-supplemented, pure culture of the green alga Scenedesmus obliquus every 3–4 days.
Morphological and life-history trait assay
Morphological and life-history characteristics were assayed using a standard experimental design [28, 55]. Briefly, single immature females were used to establish experimental lines from the stock cultures. These lines were then maintained by transferring a single, asexually-produced progeny to a new culture for two generations. Morphological and life-history measures were assayed on third generation individuals. This design minimizes the contribution of maternal and grand-maternal effects to the among-genotype component of variance . In total, twenty randomly chosen clonal lines from each lake were used in the assay, yielding a total of 140 lines (7 lakes × 20 lines).
Individuals in the experimental assay were maintained in 250 mL beakers containing 150 ml of filtered well water supplemented with S. obliquus at a concentration of 135,000 cells/mL. The water and algae mixture was replaced every other day to ensure a constant food density. Beakers were randomly assigned to trays and kept in a temperature-controlled chamber at 18°C with a photoperiod of 16L:8D. The position of trays in the chamber was changed every day to minimize micro-environmental differences.
We measured a suite of 20 morphological and life-history traits. Body-size measurements, from the top of the head to the base of the tail spine, were taken using a stereomicroscope and an optic ruler calibrated using a micrometer slide. Size was measured at birth (Sb), maturity (Sm – defined as the first instar with deposition of eggs into the brood pouch), and for three successive adult instars following maturity (S1, S2, S3). The number of offspring produced from each of the first three clutches was counted (C1, C2, C3). Clutch-specific estimates of the average body size of offspring were calculated by averaging size measures from four newborns (OS1, OS2, OS3).
During size measurements, the developmental stage of embryos in the brood chamber of mature adults, date, and time were recorded to refine estimates of the timing of maturity (Am) and adult instar durations, (A1, A2, A3) [45, 58]. The estimated time of reproductive events was then used to calculate four instar-specific estimates of growth rate: growth rate from birth to maturity (GRj); from maturity to release of first clutch (GR1); the interval between the release of first and second clutch (GR2); and the interval between the release of second and third clutch (GR3). A measure of mean adult growth rate (GRa) was calculated by averaging GR1, GR2, and GR3.
Patterns of divergence
Differences in morphological and life-history traits between Daphnia from fish and fishless lakes and among populations were assessed using nested analysis of variance (NANOVA) in which covariance parameters were estimated using restricted maximum likelihood [PROC MIXED; ]. Lake type (fish or fishless) and population nested within lake type were treated as fixed effects. We report unadjusted p-values and set our level of significance at p < 0.05. We do not adjust our level of significance based on the number of comparisons (20), but instead use conservatism in our interpretation of results.
Patterns of character change
We estimated the nature of character change for each trait with linear regression models using years exposed to fish predation as the independent variable and trait values as the dependent variable .
Rates of divergence
We calculated trait-specific rates of divergence for each of the four fish populations using haldanes and darwins [40, 58]. Haldanes are appropriate for comparisons across diverse traits and taxa because the change in means is scaled by the pooled standard deviation, causing them to be independent of trait dimensionality. Darwins represent change on an absolute scale and are influenced by trait dimensionality . We calculated haldanes to facilitate comparisons across traits within our study, and darwins, which are more commonly used than haldanes, for comparison with other studies. For both measures, the population-mean trait values and variances at time 0 were estimated by pooling all three fishless populations (Table 1). Population-mean trait values and variances for time 1 were calculated for each fish population separately. These values were used to calculate rates of divergence between fishless populations and each of the four fish populations. Our calculations of haldanes assume one sexual generation is equivalent to one year, although a sexual generation in Daphnia may span several generations of clonal reproduction.
We thank M. Kanaga, and J. Thompson for providing laboratory assistance. S. Carroll, C. Faulhaber, F. Messina, the Utah State University Evolution Group, and an anonymous reviewer provided helpful comments on the manuscript. Funding for this study was provided by NSF grant DEB-021212487, a USU New Faculty Research Grant, and a USU Center for Integrated BioSystems research grant to M. Pfrender, and NSF grant DEB-0075509 to R. Knapp and O. Sarnell.
- Kareiva PM, Kingsolver JG, Huey RB, Eds: Biotic Interactions and Global Change. 1993, Sunderland SinauerGoogle Scholar
- Purvis A, Jones KE, Mace GM: Extinction. BioEssays. 2000, 22: 1123-1133. 10.1002/1521-1878(200012)22:12<1123::AID-BIES10>3.0.CO;2-C.View ArticlePubMedGoogle Scholar
- Pease CM, Lande R, Bull JJ: A model of population growth, dispersal and evolution in a changing environment. Ecology. 1989, 70: 1657-1664. 10.2307/1938100.View ArticleGoogle Scholar
- Price TD, Qvarnstrom A, Irwin DE: The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B. 2003, 270: 1433-1440. 10.1098/rspb.2003.2372.View ArticleGoogle Scholar
- Reznick DN, Ghalambor CK: The population ecology of contemporary adaptations: what empirical studies reveal about conditions that promote adaptive evolution. Genetica. 2001, 112: 183-198. 10.1023/A:1013352109042.View ArticlePubMedGoogle Scholar
- Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O'Neil P, Parker IM, Thompson JN, Weller SG: The population biology of invasive species. Ann Rev Ecol Syst. 2001, 32: 305-332. 10.1146/annurev.ecolsys.32.081501.114037.View ArticleGoogle Scholar
- Lee CE: Evolutionary genetics of invasive species. Trends Ecol Evol. 2002, 17: 386-391. 10.1016/S0169-5347(02)02554-5.View ArticleGoogle Scholar
- Thompson JN: Rapid evolution as an ecological process. Trends Ecol Evol. 1998, 13: 329-332. 10.1016/S0169-5347(98)01378-0.View ArticlePubMedGoogle Scholar
- Carroll SP, Dingle H, Klassen SP: Genetic differences of fitness associated traits among rapidly evolving populations of the soapberry bug. Evolution. 1997, 51: 1182-1188. 10.2307/2411048.View ArticleGoogle Scholar
- Carroll SP, Klassen SP, Dingle H: Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug. Evol Ecol. 1998, 12: 955-968. 10.1023/A:1006568206413.View ArticleGoogle Scholar
- Carroll SP, Dingle H, Famula TR: Rapid appearance of epistatis during adaptive divergence following colonization. Proc R Soc Lond B. 2003, 80-83. 10.1098/rsbl.2003.0019. Suppl
- Strauss SY, Lau JA, Carroll SP: Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities?. Ecol Lett. 2006, 9: 357-374. 10.1111/j.1461-0248.2005.00874.x.View ArticlePubMedGoogle Scholar
- Reznick DN, Shaw FH, Rood FH, Shaw RG: Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science. 1997, 275: 1934-1937. 10.1126/science.275.5308.1934.View ArticlePubMedGoogle Scholar
- Johnson MTJ, Agrawal AA: The ecological play of predator-prey dynamics in an evolutionary theatre. Trends Ecol Evol. 2003, 18: 549-551. 10.1016/j.tree.2003.09.001.View ArticleGoogle Scholar
- Gil-da-Costa R, Palleroni A, Hauser MD, Touchton J, Kelley JP: Rapid acquisition of an alarm response by a neotropical primate to a newly introduced avian predator. Proc R Soc Lond B. 2003, 270: 605-610. 10.1098/rspb.2002.2281.View ArticleGoogle Scholar
- Cousyn C, De Meester L, Colbourne JK, Brendonck L, Verschuren D, Volckaert F: Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proc Natl Acad Sci USA. 2001, 98: 6256-6260. 10.1073/pnas.111606798.PubMed CentralView ArticlePubMedGoogle Scholar
- Losos JB, Schoener TW, Spiller DA: Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature. 2004, 432: 505-508. 10.1038/nature03039.View ArticlePubMedGoogle Scholar
- O'Steen S, Cullum AJ, Bennet AF: Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulate). Evolution. 2002, 56: 776-784. 10.1554/0014-3820(2002)056[0776:REOEAI]2.0.CO;2.View ArticlePubMedGoogle Scholar
- Mooney HA, Cleland EE: The evolutionary impact of invasive species. Proc Natl Acad Sci USA. 2001, 98: 5446-5451. 10.1073/pnas.091093398.PubMed CentralView ArticlePubMedGoogle Scholar
- Kolar CS, Lodge DM: Ecological predictions and risk assessment for alien fishes in North America. Science. 2002, 298: 1233-1236. 10.1126/science.1075753.View ArticlePubMedGoogle Scholar
- Simon KS, Townsend CR: Impacts of freshwater invaders at different levels of ecological organization, with emphasis on salmonids and ecosystem consequences. Fresh Biol. 2003, 48: 982-994. 10.1046/j.1365-2427.2003.01069.x.View ArticleGoogle Scholar
- Brooks JL, Dodson SI: Predation, body size, and composition of plankton. Science. 1965, 150: 28-35. 10.1126/science.150.3692.28.View ArticlePubMedGoogle Scholar
- Galbraith MG: Size-selective predation on Daphnia by Rainbow Trout and Yellow Perch. Trans Am Fish Soc. 1967, 96: 1-10. 10.1577/1548-8659(1967)96[1:SPODBR]2.0.CO;2.View ArticleGoogle Scholar
- Zaret TM, Kerfoot WC: Fish predation on Bosmina longirostris : body-size selection versus visibility selection. Ecology. 1975, 56: 232-237. 10.2307/1935317.View ArticleGoogle Scholar
- O'Brien WJ, Kettle D, Riessen H: Helmets and invisible armor: structures reducing predation from tactile and visual planktivores. Ecology. 1979, 60: 287-294. 10.2307/1937657.View ArticleGoogle Scholar
- Sprules WG: Effects of size-selective predation and food competition on high altitude zooplankton communities. Ecology. 1972, 53: 375-386. 10.2307/1934223.View ArticleGoogle Scholar
- Hairston NG, Lampert W, Cáceres CE, Holtmeir CL, Weider LJ, Gaedke U, Fischer JM, Fox JA, Post DM: Rapid evolution revealed by dormant eggs. Nature. 1999, 401: 446-10.1038/46731.View ArticleGoogle Scholar
- Pfrender ME, Lynch M: Quantitative genetic variation in Daphnia : Temporal changes in genetic architecture. Evolution. 2000, 54: 502-1509. 10.1554/0014-3820(2000)054[1502:QGVIDT]2.0.CO;2.View ArticleGoogle Scholar
- Dodson SI: Complementary feeding niches sustained by size-selective predation. Limnol Oceanogr. 1970, 15: 131-137.Google Scholar
- Wells L: Effects of alewife predation on zooplankton populations in Lake Michigan. Limnol Oceanogr. 1970, 15: 556-565.View ArticleGoogle Scholar
- Werner EE, Hall DJ: Optimal foraging and the size selection of prey by bluegill sunfish (Lepomis Macrochirus). Ecology. 1974, 55: 1042-1052. 10.2307/1940354.View ArticleGoogle Scholar
- Kitchell JA, Kitchell JF: Size-selective predation, light transmission, and oxygen stratification: Evidence from the recent sediments of manipulated lakes. Limnol Oceanogr. 1980, 25: 389-402.View ArticleGoogle Scholar
- Pijanowska J, Weider LJ, Lampert W: Predator-mediated genotypic shifts in a prey population: Experimental evidence. Oecologia. 1993, 96: 40-42. 10.1007/BF00318028.View ArticleGoogle Scholar
- Barata C, Baird DJ, Soares AMVM: Phenotypic plasticity in Daphnia magna Straus: variable maturation instar as an adaptive response to predation pressure. Oecologia. 2001, 129: 220-227. 10.1007/s004420100712.View ArticleGoogle Scholar
- Bradford DF, Cooper SD, Jenkins TM, Kratz K, Sarnelle O, Brown AD: Influences of natural acidity and introduced fish on faunal assemblages in California alpine lakes. Can J Fish Aquat Sci. 1998, 55: 2478-2491. 10.1139/cjfas-55-11-2478.View ArticleGoogle Scholar
- Knapp RA, Matthews KR, Sarnelle O: Resistance and resilience of alpine lake fauna to fish introductions. Ecol Mono. 2001, 71: 401-421. 10.2307/3100066.View ArticleGoogle Scholar
- Knapp RA, Hawkins CP, Ladau J, McClory JG: Fauna of Yosemite National Park lakes has low resistance but high resilience to fish introductions. Ecol Appl. 2005, 15: 835-847.View ArticleGoogle Scholar
- Stoddard JL: Microcrustacean communities of high-elevation lakes in the Sierra Nevada, California. J Plank Res. 1987, 9: 631-650. 10.1093/plankt/9.4.631.View ArticleGoogle Scholar
- Sarnelle O, Knapp RA: Zooplankton recovery after fish removal: limitations of the egg bank. Limnol Oceanogr. 2004, 49: 1382-1392.View ArticleGoogle Scholar
- Hendry AP, Kinnison MT: The pace of modern life: measuring rates of contemporary microevolution. Evolution. 1999, 53: 1637-1653. 10.2307/2640428.View ArticleGoogle Scholar
- Phillips BL, Shine R: Adapting to and invasive species: toxic cane todes induce morphological change in Australian snakes. Proc Natl Acad Sci USA. 2004, 101: 17150-17155. 10.1073/pnas.0406440101.PubMed CentralView ArticlePubMedGoogle Scholar
- Carroll SP, Loye JE, Dingle H, Mathieson M, Famula TR, Zalucki MP: And the beak shall inherit – evolution in response to invasion. Ecol Lett. 2005, 8: 944-951. 10.1111/j.1461-0248.2005.00800.x.View ArticleGoogle Scholar
- Declerck S, DeMeester L: Impact of fish predation on coexisting Daphnia taxa: a partial test of the temporal hybrid superiority hypothesis. Hydrobiologia. 2003, 500: 83-94. 10.1023/A:1024656602248.View ArticleGoogle Scholar
- Lynch M, Pfrender ME, Spitze K, Lehman N, Hicks J, Allan D, Latta L, Ottene M, Bogue F, Colbourne J: The quantitative and molecular genetic architecture of a subdivided species. Evolution. 1999, 53: 100-110. 10.2307/2640923.View ArticleGoogle Scholar
- Morgan KK, Hicks J, Spitze K, Latta L, Pfrender ME, Weaver CS, Ottone M, Lynch M: Patterns of genetic architecture for life-history traits and molecular markers in a subdivided species. Evolution. 2001, 55: 1753-1761. 10.1554/0014-3820(2001)055[1753:POGAFL]2.0.CO;2.View ArticlePubMedGoogle Scholar
- Gadgil M, Bossert WH: Life historical consequences of natural selection. Am Nat. 1970, 104: 1-24. 10.1086/282637.View ArticleGoogle Scholar
- Lampert W: Phenotypic plasticity of the size at first reproduction in Daphnia : the importance of maternal size. Ecology. 1993, 74: 1455-1466. 10.2307/1940074.View ArticleGoogle Scholar
- Tollrian R: Predator-induced morphological defenses: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology. 1995, 76: 1691-1705. 10.2307/1940703.View ArticleGoogle Scholar
- Mikulski A: The presence of fish induces the quick release of offspring by Daphnia. Hydrobiologia. 2001, 442: 195-198. 10.1023/A:1017542324597.View ArticleGoogle Scholar
- DeStasio BT: The seed bank of a freshwater crustacean: Copepodology for the plant ecologist. Ecology. 1989, 70: 1377-1389. 10.2307/1938197.View ArticleGoogle Scholar
- Hairston NG, Kearns CM: Temporal dispersal: Ecological and evolutionary aspects of zooplankton egg banks and the roles of sediment mixing. Integ Comp Biol. 2002, 42: 481-491. 10.1093/icb/42.3.481.View ArticleGoogle Scholar
- Lynch M, Gabrial W: Phenotypic evolution and parthenogenesis. Am Nat. 1983, 122: 745-764. 10.1086/284169.View ArticleGoogle Scholar
- Lynch M, Deng H-W: Genetic slippage in response to sex. Am Nat. 1994, 144: 242-262. 10.1086/285673.View ArticleGoogle Scholar
- Deng H-W, Lynch M: Change in genetic architecture in response to sex. Genetics. 1996, 143: 203-212.PubMed CentralPubMedGoogle Scholar
- Lynch M: Spontaneous mutations for life-history characters in an obligate parthenogen. Evolution. 1985, 39: 804-818. 10.2307/2408680.View ArticleGoogle Scholar
- Spitze K: Population-structure in Daphnia obtusa – quantitative genetic and allozymic variation. Genetics. 1993, 135: 367-374.PubMed CentralPubMedGoogle Scholar
- SAS Institute Inc Cary. 2004
- Haldane JBS: Suggestions as to quantitative measurement of rates of evolution. Evolution. 1949, 3: 51-56. 10.2307/2405451.View ArticlePubMedGoogle Scholar
- Gingerich PD: Quantification and comparison of evolutionary rates. Am J Sci. 1993, 293A: 453-478.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.