Lake-Stream Divergence in Stickleback Life History: A Plastic Response to Trophic Niche Differentiation?

Abstract

Speciation can be promoted by phenotypic plasticity if plasticity causes populations in ecologically different habitats to diverge in traits mediating reproductive isolation. Although this pathway can establish reproductive barriers immediately and without genetic divergence, it remains poorly investigated. In threespine stickleback fish, divergence in body size between populations represents a potent source of reproductive isolation because body size often influences reproductive behavior. However, the relative contribution of phenotypic plasticity and genetically based divergence to stickleback body size evolution has not been explored. We here do so by using populations residing contiguously in Lake Constance (Central Europe) and its tributaries, a system where lake fish exhibit strikingly larger size and greater age at maturity than stream fish. Laboratory experiments reveal the absence of substantial genetic divergence in intrinsic growth rates and maturation size thresholds between lake and stream fish. A field transplant experiment further demonstrates that lake fish display the life history typical of stream fish when exposed to stream habitats for one year, confirming that life history divergence in this system is mainly plastic. This plasticity appears to be driven by restricted food availability in the lake relative to the stream habitat. We thus propose that in this stickleback system, the exploitation of different trophic niches immediately promotes reproductive isolation via resource-based plasticity in life history.

Sexual isolation promotes divergence between parapatric lake and stream stickleback

“…In our experiment, lake fish were dramatically larger than their stream counterparts, a pattern consistent with field data from lake and stream stickleback in the Lake Constance basin collected in previous years (Lucek et al ., ; Moser et al ., , ). The body size differences among populations in this system largely reflect a by‐product of phenotypic plasticity in life history, presumably driven by the exploitation of differential food resources (Moser et al ., , ). Specifically, foraging on benthic prey typically permits an annual life cycle with small reproductive body size in the stream populations, whereas pelagic foraging appears less rewarding, generally allowing the lake fish to breed only after 2 years – albeit at larger size.…”

“…To confirm successful fertilization within the mesocosms, the clutches obtained at the end of 32 haphazardly chosen trials were incubated in the laboratory as in Moser et al . (). All these clutches proved well fertilized and displayed normal embryonic development.…”

“…As study populations, we used stickleback from Lake Constance, a very large and genetically well‐mixed population (Moser et al ., ; Roesti et al ., ; sampling occurred at the ROM site described in Berner et al ., ), and from a tributary to that lake (the NID stream population in Berner et al ., ). These populations exhibit highly divergent life styles (pelagic vs. benthic) and associated differentiation in trophic and predator‐mediated morphology and in life history (Berner et al ., ; Moser et al ., , ). This phenotypic differentiation is at least partly the outcome of divergent natural selection: first, a marker‐based genome scan identified numerous signatures of selection in localized genome regions between these populations (Roesti et al ., ).…”

“…S1). As nest construction material, we added to each nesting site approximately 500 green and black polyester sewing threads of 6 cm length (Barber et al ., ; Moser et al ., ), 0.8 g of filaments of the cyanobacterium Nostoc flagelliforme (‘fat choy’) and four thalli of Brachythecium sp. moss.…”

“…However, to preclude potential ambiguities, we recorded the initial body mass of all experimental males. Males not used immediately and all females were transferred to the laboratory and distributed among 20 50–120 L aquaria under long‐day (summer) conditions (details provided in Moser et al ., ), keeping the sexes separate. Both the males in the mesocosms and the laboratory fish were fed defrosted chironomid larvae (bloodworms) – the prey consumed predominantly by both study populations on breeding grounds (Moser et al ., ) – and frozen Daphnia to satiation at least twice daily.…”