Competition-Driven Speciation in Cichlid Fish
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ARTICLE Received 30 Oct 2013 | Accepted 10 Feb 2014 | Published 28 Feb 2014 DOI: 10.1038/ncomms4412 Competition-driven speciation in cichlid fish Kai Winkelmann1,2, Martin J. Genner2, Tetsumi Takahashi3 & Lukas Ru¨ber4 Theoretically, competition can initiate divergence in habitat use between individuals of a species, leading to restricted gene flow and eventual speciation. Evidence that sister species differ in habitat use is commonplace and consistent with this mechanism, but empirical experimental support is surprisingly scarce. Here we provide evidence that competition has taken a key role in the evolution of genetically distinct ecomorphs of the Lake Tanganyika cichlid fish Telmatochromis temporalis. Experiments show that differences in substrate use between a large-bodied rock-living ecomorph and a neighbouring small-bodied shell-living ecomorph are mediated by size-dependent competition that drives assortative mate-pair formation. Specifically, adults of the larger ecomorph outcompete adults of the smaller ecomorph on favoured rock substrate, compelling the smaller adults to use shell habitat. These results support a role for competition in maintaining reproductive isolation, and highlight the need to identify ecological processes that impose selection to improve our understanding of speciation and adaptive radiation. 1 Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK. 2 School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK. 3 Laboratory of Animal Ecology, Graduate School of Science, Kyoto University, Kitashirakawa-Oiwake, Kyoto 606-8502, Japan. 4 Naturhistorisches Museum der Burgergemeinde Bern, Bernastrasse 15, Bern 3005, Switzerland. Correspondence and requests for materials should be addressed to K.W. (email: [email protected]) or to M.J.G. (email: [email protected]). NATURE COMMUNICATIONS | 5:3412 | DOI: 10.1038/ncomms4412 | www.nature.com/naturecommunications 1 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms4412 he theory of ecological speciation proposes that ecologi- a cally based divergent selection leads to the evolution of Tdifferences among populations in habitat use, in turn restricting gene flow and promoting reproductive isolation1,2. Relative success of individual phenotypes on different habitat types will depend on resources available3 and ecological interactions4,5 (such as competition, predation or parasitism) that impose natural selection upon them. Examples where ecological speciation has been invoked are widespread6,7 and there is abundant phylogenetic and population genetic evidence that the speciation process is frequently associated with divergent patterns of resource use. However, it is often unclear how selection has promoted the divergence of ecomorphs and driven associated assortative mating. There is need for more thorough investigations of how natural selection operates during speciation. b c Specifically, experimental evidence of competition’s role in speciation has remained elusive8,9. This is despite the concept 10 being implicit in the work of Darwin , evidence that competition 1 2 for limited resources can restrict habitat use and geographic Lake Tanganyika 11–13 overlap of species , and signs that competition can drive 3 divergent eco-phenotypic character displacement where closely 4 related lineages occur in sympatry14,15. 5 Theoretical studies predict competition as a driving force in speciation, particularly in non-allopatric scenarios16,17. In simulations, competition has either been modelled among individuals in a single environment competing for resource along Lufubu River a single axis (for example, food), or among individuals competing for resources along an environmental gradient (for example 13 18–20 12 temperature, humidity and soil nutrients) . Evidence from the 6 11 10 resource-use patterns and spatial distributions of sister species 7 pairs in nature conform to expected outcomes of such modelled Izi 8 processes, but direct experimental evidence of competition as a 9 driving force for evolutionary diversification is notably rare. River Moreover, whether competition can directly enforce reproduction Lunzua River isolation among populations remains an open question. Figure 1 | T. temporalis from Lake Tanganyika. (a) The smaller shell In this study, we used population genetic and experimental ecomorph occupies empty shells of the gastropod N. tanganyicense. Fish evidence to demonstrate a role for competition in speciation pictured are rock (right/orange) and shell (left/yellow) ecomorph males within the cichlid fish adaptive radiation of Lake Tanganyika in from localities 10 and 11, respectively. Scale bar, 10 mm. (b) Samples for East Africa. The littoral shoreline of this lake comprises a mosaic population-level phylogenetic analyses were from 13 sites in the south of of habitats, alternating between rock, open sand, vegetation- 21,22 the lake. Orange circles ¼ rock habitat sites and yellow circles ¼ shell dominated and patchily distributed shell beds . A species habitat. Site 13 was mixed rock and shell substrate. Live fish for behavioural characteristic of the rock and shell habitats is Telmatochromis experiments were from six sites (2, 3, 4, 5, 10 and 11). Scale bar, 10 km. temporalis (Cichlidae, Lamprologini), a substrate-spawner with 23 (c) Map of Africa with the East African Great Lakes, including Lake biparental care and a lake-wide distribution . To avoid predation Tanganyika. Scale bar, 2,000 km. by other fishes, mammals or birds, it uses rock or shell substrate for shelter, egg laying and rearing young. It has two distinct ecomorphs, a large-bodied rock-morph (wild adult males: 75.7– 88.1 mm standard length (SL), wild adult females: 53.1–62.0 mm ecomorph have greater gonad size than comparably size SL) and a small-bodied shell-morph (wild adult males: 40.3– individuals of larger rock ecomorph. This suggests that 44.8 mm SL, wild adult females: 26.8–29.4 mm SL) found on shell differences in development of gonads have a genetic basis, and 23 is consistent with field observations that the shell ecomorph beds , which are dominated by empty Neothauma gastropod 23,24 shells22 (Fig. 1a). The two habitats are typically separated by matures at a smaller size than the rock ecomorph . Finally, we stretches of sand or muddy habitat24–26. Analyses of field- demonstrate using a series of controlled laboratory experiments collected samples have shown evidence of reproduction isolation that divergent habitat-use patterns, and assortative mate-pair between the T. temporalis ecomorphs23,24, and has revealed formation can be replicated in laboratory conditions, and that differences between them in reproductive biology (egg number23 habitat use is determined by size-dependent competition for and size at reproduction23) and morphology (body shape24). territorial space. Given the widespread evidence for habitat However, previous research has not identified the mechanisms differences between sister species in nature, we conclude that restricting gene flow, or tested for a genetic basis to observed competition may have a broad role in generating patterns of phenotypic differences. divergent habitat use, which in turn promotes reproductive Here we present evidence from mitochondrial DNA (mtDNA) isolation and eventual speciation. sequences and nuclear AFLP (amplified fragment length poly- morphism) markers supporting the hypothesis that the shell and Results rock ecomorphs have diverged due to evolutionary processes Evolutionary history of populations. We sampled 13 popula- operating over local spatial scales. We next demonstrate using a tions covering 170 km of shoreline and encompassing both shell common garden experiment that individuals of the smaller shell and rock habitats (Fig. 1b; Supplementary Table 1). All shell 2 NATURE COMMUNICATIONS | 5:3412 | DOI: 10.1038/ncomms4412 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms4412 ARTICLE habitats were in close proximity to rock habitat (range 20 m to for differences in gonad mass between ecomorphs (rock/shell) 2 km). We reconstructed the evolutionary relationships of sam- and sampling sites (Chibwensolo 2-3, Mbita Island 10-11, Fig. 1), pled populations using mtDNA sequences and nuclear genome- while controlling for body mass, in males and females separately. wide AFLP markers (Fig. 2, Supplementary Figs 1 and 2). The Both sexes of the shell ecomorph had significantly greater gonad results showed that the primary genetic structure was explained mass than equivalents of the rock ecomorph (analysis of by geographic separation among populations, rather than diver- covariance (ANCOVA); males F1,77 ¼ 8.714, P ¼ 0.004, shell gence between ecomorphs (Supplementary Table 2). These results males n ¼ 42, rock males n ¼ 40; females F1,84 ¼ 26.440, imply that the processes that have driven and maintained the Po0.001, shell females n ¼ 43, rock females n ¼ 46; phenotypic and genetic divergence between neighbouring Supplementary Fig. 3). There was no significant difference ecomorphs occur at the local scale and are consistent with a between the Chibwensolo or Mbita island sampling sites for pattern of parallel evolution, suggested from previous analyses of males (ANCOVA; F1,77 ¼ 2.667, P ¼ 0.106), but a significant 23,24 microsatellite and mtDNA markers . difference was present for females (ANCOVA; F1,84 ¼ 4.214, P ¼ 0.043). Although the