Developmental shifts and species selection in gastropods

Abstract

The fossil record of marine gastropods has been used as evidence to support the operation of species selection; namely, that species with limited dispersal differentially increase in numbers because they are more likely to speciate than widely dispersing species. This conclusion is based on a tacit phylogenetic assumption that increases in species with limited dispersal are solely the result of speciation within monophyletic groups with low dispersal. To test this assumption, we reconstructed a phylogeny from nuclear sequence data for 70 species of the marine gastropod genus Conus and used it to map the evolution of developmental mode. All eight species without planktonic life history phases recently and independently evolved this characteristic from ancestors with planktonic larval phases, showing that transitions in developmental mode are common in this group. A simple model of species diversification shows that such shifts can control the relative numbers of species with and without dispersing larval stages, leading to apparent species selection. Such results challenge the conclusion that increases in the number of nonplanktonic species relative to species with planktonic larvae over geologic time is necessarily a result of higher rates of speciation of nonplanktonic lineages and show that demonstration of species selection requires a phylogenetic framework.

Figure 1

Models of the evolutionary history of a group of species with interspecific variation in a character that may affect speciation and extinction rates of lineages. (A) No higher order effect. Transitions in the character state of this character occur commonly. Species with these traits (bold lines) do not form monophyletic groups. Species selection does not produce any observed pattern of trait variation among fossil assemblages. (B) Very few (one) transitions in character state. Different character states affect species’ origination rates. Species with similar traits form monophyletic groups. Species selection in this case could change the frequency of this trait among species over time.

Figure 2

Neighbor-joining tree reconstructed from calmodulin intron sequence data of Conus. Bootstrap values indicated on branches. Bootstrap values less than 50% were omitted. Names in italics are species whose developmental mode is unknown. Names shaded in gray are nonplanktonic species. All names in normal typeface are species with a planktonic larval phase.

Figure 3

Developmental shifts can mimic the effects of species selection. Simulated trajectories of the numbers of nonplanktonic species relative to the total number of species. Each run started with 50 species with planktonic larvae and one nonplanktonic species and consisted of 100 opportunities for speciation, extinction, or transition of developmental mode. Speciation and extinction probabilities (0.25) are identical for species with each developmental mode and were allowed to independently vary randomly within 10% of the mean probability. Transition probability was set to 0.05 and was allowed to vary randomly within 10% of this value.