A millennial‐scale chronicle of evolutionary responses to cultural eutrophication in Daphnia

Abstract

For an accurate assessment of the anthropogenic impacts on evolutionary change in natural populations, we need long-term environmental, genetic and phenotypic data that predate human disturbances. Analysis of c. 1600 years of history chronicled in the sediments of South Center Lake, Minnesota, USA, revealed major environmental changes beginning c. 120 years ago coinciding with the initiation of industrialised agriculture in the catchment area. Population genetic structure, analysed using DNA from dormant eggs of the keystone aquatic herbivore, Daphnia pulicaria, suggested no change for c. 1500 years prior to striking shifts associated with anthropogenic environmental alterations. Furthermore, phenotypic assays on the oldest resurrected metazoan genotypes (potentially as old as c. 700 years) indicate significant shifts in phosphorus utilisation rates compared to younger genotypes. Younger genotypes show steeper reaction norms with high growth under high phosphorus (P), and low growth under low P, while 'ancient' genotypes show flat reaction norms, yet higher growth efficiency under low P. Using this resurrection ecology approach, environmental, genetic and phenotypic data spanning pre- and post-industrialised agricultural eras clearly reveal the evolutionary consequences of anthropogenic environmental change.

Monogonont rotifers as model systems for the study of micro-evolutionary adaptation and its eco-evolutionary implications

“…With diapausing eggs, populations can survive adverse conditions and disperse both in space and time. A nice feature of these eggs is that they can be used to reconstruct evolutionary trajectories of natural populations through time via the 'resurrection' of genotypes that may be recovered from stratified lake sediments (Kerfoot et al, 1999;Decaestecker et al, 2007;Frisch et al, 2014).…”

Seventy five years of limnology at the Istituto Italiano di Idrobiologia in Pallanza

“…A sediment section dating back half a century ago, for example, allows for comparing life history patterns of organisms from around 1500 generations ago with respect to those currently living in the same environment. The span of living eggs retrieved from sediment cores conforms nicely to the time frame of microevolutionary responses (i.e., multiple generations), therefore offering indirect evidence for microevolutionary changes along with environmental conditions (e.g., Kerfoot and Weider, 2004;Frisch et al, 2014).…”

“…The discovery of sediment cores as a source for resurrecting organisms from the past (resurrection ecology; Kerfoot et al, 1999;Kerfoot and Weider, 2004;Frisch et al, 2014), offers a unique opportunity for quantifying changes in diversity, taxa composition and life strategies of aquatic populations in response to natural and anthropogenic disturbances, adding a dynamic dimension to palaeolimnology (Jeppesen et al, 2001;Guilizzoni, 2012). The hatching of ephippial eggs isolated from sediments of a known age allows for reconstructing changes in life history traits associated with environmental perturbations, included exposure to toxic conditions.…”

“…Resurrecting ancestors for transgenerational tests represents a new experimental approach to paleolimnology, answering the vexing question of how to test paleolimnological inferences directly (Kerfoot and Weider, 2004). Indirect estimates of past populations to compare their performance with respect to contemporary ones, under past and present conditions allow for detecting changes in level of tolerance along with, and for identifying mechanisms responsible for the essential ability of species/clones to compete and survive under different perturbations, included heavy metal pollution (Piscia et al, 2014;Frisch et al, 2014).…”

Experimental macroevolution

“…In lakes with varved sediments, a time series of dormant propagules can be isolated from cores, with some assurance that the sediments have not been mixed by burrowing animals ( [15,16]; reviewed by Orsini et al [17]). Germinating the dormant embryos ('ephippia') of cladocerans has made it possible to trace rapid evolutionary change [18], for example adaptation to historical eutrophication during the past 700 years [19,20].…”