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ABSTRACT Colonization of a novel habitat is often followed by radiation in the wake of ecological opportunity. Alternatively, some habitats should be inherently more constraining than others if the challenges of that environment have few evolutionary solutions. We examined the push-and-pull of these factors on evolution following habitat transitions, using anglerfishes (Lophiiformes) as a model. Deep-sea fishes are notoriously difficult to study, and poor sampling has limited progress thus far. Here we present a new phylogeny of anglerfishes with unprecedented taxonomic sampling (1,092 loci and 40% of species), combined with three-dimensional phenotypic data from museum specimens obtained with micro-CT scanning. We use these datasets to examine the tempo and mode of phenotypic and lineage diversification using phylogenetic comparative methods, comparing lineages in shallow and deep benthic versus bathypelagic habitats. Our results show that anglerfishes represent a surprising case where the bathypelagic lineage has greater taxonomic and phenotypic diversity than coastal benthic relatives. This defies expectations based on ecological principles since the bathypelagic zone is the most homogeneous habitat on Earth. Deep-sea anglerfishes experienced rapid lineage diversification concomitant with colonization of the bathypelagic zone from a continental slope ancestor. They display the highest body, skull and jaw shape disparity across lophiiforms. In contrast, reef-associated taxa show strong constraints on shape and low evolutionary rates, contradicting patterns suggested by other shallow marine fishes. We found that Lophiiformes as a whole evolved under an early burst model with subclades occupying distinct body shapes. We further discuss to what extent the bathypelagic clade is a secondary adaptive radiation, or if its diversity can be explained by non-adaptive processes. 

Body size is an important species trait, correlating with life span, fecundity, and other ecological factors. Over Earth’s geological history, climate shifts have occurred, potentially shaping body size evolution in many clades. General rules attempting to summarize body size evolution include Bergmann’s rule, which states that species reach larger sizes in cooler environments and smaller sizes in warmer environments, and Cope’s rule, which poses that lineages tend to increase in size over evolutionary time. Tetraodontiform fishes (including pufferfishes, boxfishes, and ocean sunfishes) provide an extraordinary clade to test these rules in ectotherms owing to their exemplary fossil record and the great disparity in body size observed among extant and fossil species. We examined Bergmann’s and Cope’s rules in this group by combining phylogenomic data (1,103 exon loci from 185 extant species) with 210 anatomical characters coded from both fossil and extant species. We aggregated data layers on paleoclimate and body size from the species examined, and inferred a set of time-calibrated phylogenies using tip-dating approaches for downstream comparative analyses of body size evolution by implementing models that incorporate paleoclimatic information. We found strong support for a temperature-driven model in which increasing body size over time is correlated with decreasing oceanic temperatures. On average, extant tetraodontiforms are two to three times larger than their fossil counterparts, which otherwise evolved during periods of warmer ocean temperatures. These results provide strong support for both Bergmann’s and Cope’s rules, trends that are less studied in marine fishes compared to terrestrial vertebrates and marine invertebrates. 

Abstract The development of paired appendages was a key innovation during evolution and facilitated the aquatic to terrestrial transition of vertebrates. Largely derived from the lateral plate mesoderm (LPM), one hypothesis for the evolution of paired fins invokes derivation from unpaired median fins via a pair of lateral fin folds located between pectoral and pelvic fin territories 1 . Whilst unpaired and paired fins exhibit similar structural and molecular characteristics, no definitive evidence exists for paired lateral fin folds in larvae or adults of any extant or extinct species. As unpaired fin core components are regarded as exclusively derived from paraxial mesoderm, any transition presumes both co-option of a fin developmental programme to the LPM and bilateral duplication 2 . Here, we identify that the larval zebrafish unpaired pre-anal fin fold (PAFF) is derived from the LPM and thus may represent a developmental intermediate between median and paired fins. We trace the contribution of LPM to the PAFF in both cyclostomes and gnathostomes, supporting the notion that this is an ancient trait of vertebrates. Finally, we observe that the PAFF can be bifurcated by increasing bone morphogenetic protein signalling, generating LPM-derived paired fin folds. Our work provides evidence that lateral fin folds may have existed as embryonic anlage for elaboration to paired fins.