Environmental change explains cichlid adaptive SEE COMMENTARY radiation at Lake Malawi over the past 1.2 million years Sarah J. Ivorya,b,1, Margaret W. Blomec, John W. Kingd, Michael M. McGlueb, Julia E. Colee, and Andrew S. Cohene aDepartment of Earth, Environmental, and Planetary Sciences, Brown University, Providence, RI 02912; bDepartment of Earth and Environmental Sciences, University of Kentucky, Lexington, KY 40506; cBritish Petroleum, Houston, TX 77079; dCoastal Institute, University of Rhode Island, Kingston, RI 02881; and eDepartment of Geosciences, University of Arizona, Tucson, AZ 85721 Edited by John P. Smol, Queen’s University, Kingston, Canada, and accepted by Editorial Board Member David Jablonski August 12, 2016 (received for review July 6, 2016) Long paleoecological records are critical for understanding evolu- outcrops provide only intermittent snapshots, and it is difficult to tionary responses to environmental forcing and unparalleled tools tease apart the influence of climatic versus geomorphic or tectonic for elucidating the mechanisms that lead to the development of processes. Furthermore, to integrate climate history in un- regions of high biodiversity. We use a 1.2-My record from Lake derstanding ecological and evolutionary records, distant sources of Malawi, a textbook example of biological diversification, to docu- climate information, such as marine sediment cores, are of limited ment how climate and tectonics have driven ecosystem and evolu- value for interpreting in situ processes (6, 7). Thus, long continuous tionary dynamics. Before ∼800 ka, Lake Malawi was much shallower records that preserve ecological, climatic, and sedimentological than today, with higher frequency but much lower amplitude water- indicators from within lakes are crucial to disentangling sensitivity level and oxygenation changes. Since ∼800 ka, the lake has experi- thresholds and observing environmental and evolutionary change. enced much larger environmental fluctuations, best explained by a Here we use a suite of paleoecological and mineralogical records punctuated, tectonically driven rise in its outlet location and level. from a 380-m drill core (MAL05-1B) from Lake Malawi Following the reorganization of the basin, a change in the pacing of (Fig. 1; 590-m water depth; 11°18′S, 34°26′E), in southeastern hydroclimate variability associated with the Mid-Pleistocene Transi- Africa, to reconstruct its ecosystem and limnological history tion resulted in hydrologic change dominated by precession rather over the last 1.2 My (SI Appendix, Figs. S8–S10 and Table S2) than the high-latitude teleconnections recorded elsewhere. During (5). Lake Malawi houses more fish species than any other this time, extended, deep lake phases have abruptly alternated with lake on Earth, including ∼800 cichlid species, and is an iconic times of extreme aridity and ecosystem variability. Repeated cross- “laboratory” for testing questions about rates, modes, and ings of hydroclimatic thresholds within the lake system were critical drivers of evolution (8). The lake is deep (706 m), old (>5 My), for establishing the rhythm of diversification, hybridization, and ex- and permanently stratified with a large watershed (94,000 km2), tinction that dominate the modern system. The chronology of these and preserves an excellent long sedimentological record changes closely matches both the timing and pattern of phylogenetic (9). Furthermore, its location at the southernmost seasonal ’ history inferred independently for the lake s extraordinary array of reach of the Intertropical Convergence Zone (ITCZ) and its cichlid fish species, suggesting a direct link between environmental effective moisture sensitivity make it a promising archive for and evolutionary dynamics. reconstructing regional hydroclimate and paleoecology. Previous tropical climate | cichlid evolution | adaptive radiation | paleoclimate | Significance paleoecology EVOLUTION Tropical African lakes are well-known to house exceptionally bio- econstructing hydroclimate variability in the tropics is im- diverse assemblages of fish and other aquatic fauna, which are Rportant for understanding how ecosystems have evolved and to thought to be at risk in the future. Although the modern assem- predict future environmental tipping points that may negatively blages are well-studied, direct evidence of the origin of this in- impact freshwater resources and aquatic ecosystems (1). This un- credible wealth of species and the mechanisms that drive speciation derstanding is particularly important in Africa, where incredibly are virtually unknown. We use a long sedimentary record from biodiverse aquatic ecological assemblages support a food web that Lake Malawi to show that over the last 1.2 My both large-scale is a critical staple for millions of people and access to fresh water is climatic and tectonic changes resulted in wet–dry transitions that SCIENCES limited (2). However, an enormous data gap exists in African cli- led to extraordinary habitat variability and rapid diversification ENVIRONMENTAL mate and ecosystem history, precluding a fundamental un- events. This work allows us to understand the environmental ’ derstanding of these systems sensitivity to various environmental context of aquatic evolution in the most biodiverse tropical lake. perturbations. Continuous lacustrine sedimentary records that re- veal ancient physical processes and ecosystem dynamics are Author contributions: S.J.I., M.W.B., J.W.K., M.M.M., and A.S.C. designed research; S.J.I., emerging as a unique tool that can help us understand the impli- M.W.B., J.W.K., M.M.M., and A.S.C. performed research; M.W.B., J.W.K., J.E.C., and A.S.C. cations of hydrologic thresholds and changes in aquatic ecosystem contributed new reagents/analytic tools; S.J.I., M.W.B., J.W.K., M.M.M., J.E.C., and A.S.C. analyzed data; and S.J.I., M.W.B., J.W.K., M.M.M., J.E.C., and A.S.C. wrote the paper. variability. Long and highly resolved paleorecords are also critical The authors declare no conflict of interest. for elucidating the dynamics and potential drivers of explosive speciation, which characterizes many of these ancient lakes (3). This article is a PNAS Direct Submission. J.P.S. is a Guest Editor invited by the Editorial Board. Over the Quaternary, the Afrotropics have undergone large- Data deposition: Raw ostracod data are included in figure form in SI Appendix,and tabulated data have been archived at the National Center for Climate Data (https:// scale gradual and periodic climate changes, including regional www.ncdc.noaa.gov/data-access/paleoclimatology-data/datasets); all core metadata are wet–dry cycles regulated by the magnitude of insolation forcing available at www.ngdc.noaa.gov/geosamples/showsample.jsp?imlgs=imlgs0195811. related to orbital eccentricity (4, 5). We hypothesize that these See Commentary on page 11654. events and changes in the variability of lake-level fluctuations 1To whom correspondence should be addressed. Email: [email protected]. influenced the timing of diversification of biodiverse endemic This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. faunas. However, discontinuous and poorly dated records from 1073/pnas.1611028113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1611028113 PNAS | October 18, 2016 | vol. 113 | no. 42 | 11895–11900 Downloaded by guest on October 1, 2021 Fig. 1. Map of Africa with the location of Lake Malawi with respect to July and January ITCZ positions. (Inset) Topographic map of Lake Malawi and its watershed, including the Ruhuhu River. The red dot indicates the core location. paleoecological studies have demonstrated that the lake’sbiotahas evaluate the frequency of hydroclimate variability (SI Appendix,Figs. undergone dramatic changes in the past 140 ky, which are strongly S1–S7 and Table S1). correlated with water chemistry, availability of clear-water, rocky, A principal component (PC) analysis of all hydrologically and littoral habitats, and water-column stratification changes (4, 10). sensitive fossil and mineralogical indicators shows a first-order Here we extend that record for fossil ostracode crustaceans, fish, change in the frequency and amplitude associated with lake state silicified green algae, lake flies, charred particles, and various min- starting about 800 ka (Fig. 2 and SI Appendix, Figs. S8–S10). eralogical indicators over the ∼1.2-My core record. Before that time, ostracode assemblages dominated by the freshwater Sclerocypris jenkinae and marsh/riverine Ilyocypris Results and Discussion (mostly I. alta) are observed. These ostracodes, in combination Prior studies of the MAL05-1B core from Lake Malawi lacked age with abundant freshwater mollusks, sedge pollen, and framboidal control over large portions of the record (5). In this study, we present pyrite (typical of sediment reduction in areas of high biological data with a refined age model that uses paleomagnetic excursion and oxygen demand), are correlated with negative PC1 values. This intensity records, thus allowing us to attribute timing to events and assemblage indicates direct river influence with through-flowing, Fig. 2. Lake Malawi paleoenvironments with global/regional records for the last 1.2 My. (Left to Right) First principal component of biogenic and mineralogical facies from MAL05-1B from this study, first principal component of physical properties (5) from MAL05-1B (both associated with lake-level variability), percent near monospecific Limnocythere ostracodes,