Species selection favors dispersive larvae in marine life cycles.

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For 40 years, the prevailing paradigm in evolutionary biology has been that lineages with less-dispersive, non-feeding larvae (lecithotrophs) out-diversify taxa with dispersive, feeding larvae (planktotrophs).  This theory grew out of paleontological studies performed in the 1970s and 1980s.  Based on the fossil record of select neogastropod families, six influential studies (cited >1,400 times) concluded that lecithotrophic taxa speciated at a higher rate because they accumulated over time compared to planktotrophs in the same family.  This was interpreted as evidence for species-level selection, which can be triggered by evolutionary change in a key trait; the “character state” of a trait may evolve, for instance from dispersive to non-dispersive larvae, and thereby affect the evolutionary success of a lineage.  Character change triggers species selection if lineages in one state out-diversify (radiate into more descendant species than) related lineages with a different character state.  Despite resurgent interest in understanding species selection, convincing examples are few.  Larval type in marine gastropods became a textbook example of species selection, or selection above the species level, but our work challenges this interpretation. 

 

Two primary concerns emerged during our study of classic work on this topic.  First, early studies never calculated net diversification rate (speciation – extinction), focusing only on changes in speciation rate.  Paleontological evidence indicated that both speciation and extinction rates increased for lecithotrophs; if extinction rates increased more than speciation rates, that would result in species selection favoring planktotrophs. Second, noted as early as 1992, paleontological studies did not correct for character change; phylogenetic evidence in diverse groups indicates that lecithotrophy evolves often and independently.  If planktotrophs frequently evolve into lecithotrophs by character change, then some apparent extinctions of planktotrophs in the fossil record will reflect instead their transitions to lecithotrophy; likewise, some origins of lecithotrophs attributed to speciation would also reflect character change in a planktotrophic ancestor.

 

We performed the first formal test of the hypothesis that species selection favors the less dispersive strategy of lecithotrophy using comparative methods, a four-gene phylogeny of 202 species in clade Sacoglossa, and developmental data for 114 species. Contrary to prevailing theory, planktotrophy is favored by species selection: planktotrophs significantly out-diversified lecithotrophs, which arose primarily through recent character change and went extinct before diversifying. The loss of dispersal is often favored at ecological timescales, thus lecithotrophy evolves frequently, but less dispersive strategies are strongly selected against over macroevolutionary time scales. Short-lived larvae thus produce short-lived lineages in Sacoglossa, and potentially in most invertebrate groups. Our results challenge longstanding assumptions about marine life-history evolution, yet explain why a majority of species are planktotrophic despite a high rate of conversion to lecithotrophy via character change; if lecithotrophs arose often, and also diversified more, they should predominate in most groups (but do not).

 

Krug et al. 2015, Systematic Biology 64: 983–999.               Dryad data repository