Fast adaptive responses in the oral jaw of Lake Victoria cichlids

Abstract

Rapid morphological changes in response to fluctuating natural environments are a common phenomenon in species that undergo adaptive radiation. The dramatic ecological changes in Lake Victoria provide a unique opportunity to study environmental effects on cichlid morphology. This study shows how four haplochromine cichlids adapted their premaxilla to a changed diet over the past 30 years. Directly after the diet change toward larger and faster prey in the late 1980s, the premaxilla (upper jaw) changed in a way that is in agreement with a more food manipulating feeding style. During the 2000s, two zooplanktivorous species showed a reversal of morphological changes after returning to their original diet, whereas two other species showed no reversal of diet and morphology. These rapid changes indicate a potential for extremely fast adaptive responses to environmental fluctuations, which are likely inflicted by competition release and increase, and might have a bearing on the ability of haplochromines to cope with environmental changes. These responses could be due to rapid genetic change or phenotypic plasticity, for which there is ample evidence in cichlid fish structures associated with food capture and processing. These versatile adaptive responses are likely to have contributed to the fast adaptive radiation of haplochromines.

Changing ecology of Lake Victoria cichlids and their environment: evidence from C13 and N15 analyses

“…From the 1980s onwards, several studies have shown increased nitrogen and phosphorus loadings in the lake coinciding with decreased water transparency and oxygen levels (Mugidde, 1993;Hecky et al, 1994Hecky et al, , 2010Seehausen et al, 1997a;Verschuren et al, 2002). The eutrophication is thought to be caused by agricultural malpractices, urbanization and deforestation, although recent studies have suggested that climatic variability and wind stress played a crucial role as well (Kolding et al, 2008;Hecky et al, 2010;van Rijssel, 2014). Most of the studies reporting eutrophication focussed on the northern part of the lake (Hecky, 1993;Mugidde, 1993;Mugidde et al, 2003) and because of the lack of regular and consistent measurements of biological productivity, paleolimnological analysis was used to provide more continuous analysis of historical changes in the ecosystem.…”

“…For the Mwanza Gulf, located in the southern part of the lake, even less data on productivity are available (Akiyama et al, 1977;Shayo et al, 2011;Cornelissen et al, 2014), although other environmental variables such as dissolved oxygen levels and Secchi depth data have been measured on a fairly regular basis in the last four decades (van Rijssel, 2014). In addition, the Lake Victoria biodiversity crisis has been well documented for the Mwanza Gulf from the 1970s onwards (Witte et al, 2007).…”

“…Together with the eutrophication, the Nile perch boom caused a major decline of cichlid species (Witte et al, 1992;Seehausen et al, 1997a;Goudswaard et al, 2008). However, during the 1990s, some cichlid species, especially zooplanktivores and detritivores, recovered (Seehausen et al, 1997b;Witte et al, 2007;KisheMachumu et al, 2015) and shifted their diet towards macroinvertebrates and fish (Van Oijen & Witte, 1996Katunzi et al, 2003Kishe-Machumu et al, 2008;van Rijssel et al, 2015). With the use of formalinpreserved cichlid specimens collected over the past 35 years, we demonstrated that the recovered species showed morphological adaptive responses to the environmental changes Van der Meer et al, 2012;Van Rijssel & Witte, 2013;van Rijssel et al, 2015).…”

“…laparogramma Greenwood & Gee 1969 (lap), the zooplankti/insectivorous species H. tanaos van Oijen 1996 (tan) and the mollusci/detritivorous species Platytaeniodus degeniBoulenger 1906(deg). Dietary gut content analyses revealed that the species pyr and lap shifted their diet towards large macroinvertebrates such as aquatic insects, shrimps and molluscs as well as to fish during the 1990s, but reverted their diet (partly) back to zooplankton in the 2000s which is their original diet (Katunzi et al, 2003;KisheMachumu, 2012;van Rijssel et al, 2015). These two species also extended their habitat to shallower waters (Seehausen et al, 1997b;Kishe-Machumu et al, 2015).…”

“…Dietary gut content analyses revealed that the species pyr and lap shifted their diet towards large macroinvertebrates such as aquatic insects, shrimps and molluscs as well as to fish during the 1990s, but reverted their diet (partly) back to zooplankton in the 2000s which is their original diet (Katunzi et al, 2003;KisheMachumu, 2012;van Rijssel et al, 2015). These two species also extended their habitat to shallower waters (Seehausen et al, 1997b;Kishe-Machumu et al, 2015). The species tan and deg both showed the most pronounced diet changes towards macroinvertebrates and fish during the 2000s and have extended their habitat to deeper waters (Van Oijen & Witte, 1996;Seehausen et al, 1997b;Kishe-Machumu et al, 2015;van Rijssel et al, 2015).…”