Delayed Adaptive Radiation among New Zealand Stream Fishes: Joint Estimation of Divergence Time and Trait Evolution in a Newly Delineated Island Species Flock

Abstract

Adaptive radiations are generally thought to occur soon after a lineage invades a region offering high levels of ecological opportunity. However, few adaptive radiations beyond a handful of exceptional examples are known, so a comprehensive understanding of their dynamics is still lacking. Here, we present a novel case of an island species flock of freshwater fishes with a radically different tempo of adaptive history than that found in many popular evolutionary model systems. Using a phylogenomic data set combined with simultaneous Bayesian estimation of divergence times and trait-based speciation and extinction models, we show that the New Zealand Gobiomorphus gudgeons comprise a monophyletic assemblage, but surprisingly, the radiation did not fully occupy freshwater habitats and explosively speciate until more than 10 myr after the lineage invaded the islands. This shift in speciation rate was not accompanied by an acceleration in the rate of morphological evolution in the freshwater crown clade relative to the other species, but is correlated with a reduction in head pores and scales as well as an increase in egg size. Our results challenge the notion that clades always rapidly exploit ecological opportunities in the absence of competing lineages. Instead, we demonstrate that adaptive radiation can experience a slow start before undergoing accelerated diversification and that lineage and phenotypic diversification may be uncoupled in young radiations. [Adaptive radiation; Eleotridae; freshwater; Gobiomorphus; New Zealand.].

Figure 1.

Consistent phylogenomic topology of relationships among Gobiomorphus species and outgroups. This topology was obtained in all analyses: RAxML, ExaBayes, and ASTRAL multispecies coalescent. All nodes were supported at boostrap in the RAxML analysis except those among G. basalis north, G. cotidanus, and G. alpinus, as shown. All nodes in ExaBayes and ASTRAL analyses were supported with a posterior probability of 1. Images of Gobiomorphus species are specimens from the collection of Te Papa Tongarewa, the National Museum of New Zealand: G. hubbsi (NMNZ P.058616), G. huttoni (NMNZ P.037510), G. gobioides (NMNZ P.056515), G. breviceps south (NMNZ P.004596), G. breviceps north (NMNZ P. 004441), G. basalis south (NMNZ P.058915), G. basalis north (NMNZ P.058870), G. cotidianus (NMNZ P.012637), and G. alpinus (NMNZ P.003109). Images are not scaled to actual size; G. gobioides is the largest species, reaching lengths of 24.0 cm, whereas the other species range from 7.5 to 15.8 cm in length (McDowall 2000).

Figure 2.

Joint estimation of divergence time and diversification rates in New Zealand Gobiomorphus and close relatives. DensiTree visualization shows 500 ultrametric trees sampled from the posterior of our BiSSE model. A bar indicates the age range of Miocene Gobiomorphus fossils from New Zealand. Lower panels depict probability density distributions of speciation rate (left) and extinction rate (right) for amphidromous (blue) and freshwater resident (green) lineages. Tip symbols indicate a freshwater or amphidromous lifecycle; note that one freshwater species, G. cotidianus, can also utilize an amphidromous lifecycle in some populations. Each species’ occurrence data are superimposed on a map of New Zealand, showing predominantly coastal populations of the amphidromous species not able to form freshwater resident populations but full invasion New Zealand’s freshwater habitats by the species that can.

Figure 3.

Phylomorphospace (plot of PC1 vs. PC2 with phylogeny superimposed) for Gobiomorphus species. Fish images are the same as those used in Figure 1. The species that can establish resident freshwater populations are highlighted in green; amphidromous species are highlighted in blue. The amphidromous species are arrayed to the upper right of the phylomorphospace, with the most elongate and slender species (G. hubbsi) the most divergent from the remainder. Freshwater resident species are generally more stout and compact and are clustered in the lower-left portion of the phylomorphospace.

Figure 4.

LTT and DTT plots for Gobiomorphus. LTT plots are shown in a and d. a) LTT curve for New Zealand species, superimposed on phylogeny. d) LTT curve shown over the range of results for 1000 randomly selected topologies from the RevBayes posterior distribution. DTT plots (b, c, e, and f) for PC axes show the observed DTT (solid line) superimposed on the DTT calculated on a set of 1000 trees (mean value represented by the dotted line, gray zone = and quantiles). b) DTT plot for PC1. c) DTT plot for PC2. e) DTT plot for PC3. f) DTT plot for PC4.