On the measurement of ecological novelty: scale-eating pupfish are separated by 168 my from other scale-eating fishes

Abstract

The colonization of new adaptive zones is widely recognized as one of the hallmarks of adaptive radiation. However, the adoption of novel resources during this process is rarely distinguished from phenotypic change because morphology is a common proxy for ecology. How can we quantify ecological novelty independent of phenotype? Our study is split into two parts: we first document a remarkable example of ecological novelty, scale-eating (lepidophagy), within a rapidly-evolving adaptive radiation of Cyprinodon pupfishes on San Salvador Island, Bahamas. This specialized predatory niche is known in several other fish groups, but is not found elsewhere among the 1,500 species of atherinomorphs. Second, we quantify this ecological novelty by measuring the time-calibrated phylogenetic distance in years to the most closely-related species with convergent ecology. We find that scale-eating pupfish are separated by 168 million years of evolution from the nearest scale-eating fish. We apply this approach to a variety of examples and highlight the frequent decoupling of ecological novelty from phenotypic divergence. We observe that novel ecology is not always tightly correlated with rates of phenotypic or species diversification, particularly within recent adaptive radiations, necessitating the use of additional measures of ecological novelty independent of phenotype.

Figure 1. Illustration of the phylogenetic novelty index applied to scale-eating in Cyprinodon sp. ‘bulldog’.

The most closely related species with convergent ecology are a clade of scale-eating cichlids from Lake Tanganyika, Perissodus spp. A simplified cladogram connecting these groups is illustrated with numbers at tips corresponding to the number of scale-eating (black) and non-scale-eating (red) species within the Cyprinodon and Tanganyikan haplochromine clades (note that thousands of additional outgroup species have been pruned and these species numbers are not presented). Phylogenetic novelty index (indicated by the green line; 168 million years in Table 3) is calculated from twice the divergence time (t) minus the estimated origin of scale-eating in each clade (a and b). The stem age of the Perissodus clade is used as a conservative estimate of the origin of scale-eating (b). Note that the phylogenetic novelty index is not the same if applied to scale-eating cichlids (Table 3), which have repeatedly colonized this niche within each Great Lake radiation. Also note the aggressive mimicry in Perissodus straelini and the crypsis of female Cyprinodon sp. ‘bulldog’. Photo credits: Jennifer O. Reynolds, Tony Terceira.

Figure 2. Diets of Cyprinodon sp. ‘bulldog’ (red), C. sp. ‘durophage’ (green), and C. sp. ‘normal’ (blue) in two hypersaline lakes on San Salvador Island, Bahamas.

a,b) Proportion of scales (mean ± SE) in stomach contents of each species in a) Crescent Pond and b) Little Lake populations. c,d) Relative trophic position (δ¹⁵N: mean ± SE) of each species from samples collected in March (first bar) and July (second bar) in a) Crescent Pond and b) Little Lake populations. Multiple samples of ‘bulldog’ and ‘durophage’ were not available in March in Little Lake.