Correlated Evolution of Sex Allocation and Mating System in Wrasses and Parrotfishes.

In accordance with predictions of the size-advantage model, comparative evidence confirms that protogynous sex change is lost when mating behavior is characterized by weak size advantage. However, we lack comparative evidence supporting the adaptive significance of sex change. Specifically, it remains unclear whether increasing male size advantage induces transitions to protogynous sex change across species, as it can within species. We show that in wrasses and parrotfishes (Labridae) the evolution of protogynous sex change is correlated with polygynous mating and that the degree of male size advantage expressed by polygynous species influences transitions between different types of protogynous sex change. Phylogenetic reconstructions reveal strikingly similar patterns of sex allocation and mating system evolution with comparable lability. Despite the plasticity of sex-determination mechanisms in labrids, transitions trend toward monandry (all males derived from sex-changed females), with all observed losses of protogyny accounted for by shifts in the timing of sex change to prematuration. Likewise, transitions in mating system trend from the ancestral condition of lek-like polygyny toward greater male size advantage, characteristic of haremic polygyny. The results of our comparative analyses are among the first to confirm the adaptive significance of sex change as described by the size-advantage model.

Colour pattern divergence in reef fish species is rapid and driven by both range overlap and symmetry.

Signal divergence is an important process underpinning the diversification of lineages. Research has shown that signal divergence is greatest in species pairs that possess high geographic range overlap. However, the influence of range-size differences within pairs is less understood. We investigated how these factors have shaped signal divergence within brightly coloured coral reef butterflyfishes (genus: Chaetodon). Using a novel digital imaging methodology, we quantified both colouration and pattern using 250 000 sample points on each fish image. Surprisingly, evolutionary age did not affect colour pattern dissimilarity between species pairs, with average differences arising in just 300 000 years. However, the effect of range overlap and range symmetry was significant. Species-pair colour patterns become more different with increasing overlap, but only when ranges are similar in size. When ranges differ markedly in area, species-pair colour patterns become more similar with increasing overlap. This suggests that species with small ranges may maintain non-colour-based species boundaries.

Ecology shapes the evolutionary trade-off between predator avoidance and defence in coral reef butterflyfishes.

Antipredator defensive traits are thought to trade-off evolutionarily with traits that facilitate predator avoidance. However, complexity and scale have precluded tests of this prediction in many groups, including fishes. Using a macroevolutionary approach, we test this prediction in butterflyfishes, an iconic group of coral reef inhabitants with diverse social behaviours, foraging strategies and antipredator adaptations. We find that several antipredator traits have evolved adaptively, dependent primarily on foraging strategy. We identify a previously unrecognised axis of diversity in butterflyfishes where species with robust morphological defences have riskier foraging strategies and lack sociality, while species with reduced morphological defences feed in familiar territories, have adaptations for quick escapes and benefit from the vigilance provided by sociality. Furthermore, we find evidence for the constrained evolution of fin spines among species that graze solely on corals, highlighting the importance of corals, as both prey and structural refuge, in shaping fish morphology.

The role of peripheral endemism in species diversification: evidence from the coral reef fish genus Anampses (Family: Labridae).

We examined how peripherally isolated endemic species may have contributed to the biodiversity of the Indo-Australian Archipelago biodiversity hotspot by reconstructing the evolutionary history of the wrasse genus Anampses. We identified three alternate models of diversification: the vicariance-based 'successive division' model, and the dispersal-based 'successive colonisation' and 'peripheral budding' models. The genus was well suited for this study given its relatively high proportion (42%) of endemic species, its reasonably low diversity (12 species), which permitted complete taxon sampling, and its widespread tropical Indo-Pacific distribution. Monophyly of the genus was strongly supported by three phylogenetic analyses: maximum parsimony, maximum likelihood, and Bayesian inference based on mitochondrial CO1 and 12S rRNA and nuclear S7 sequences. Estimates of species divergence times from fossil-calibrated Bayesian inference suggest that Anampses arose in the mid-Eocene and subsequently diversified throughout the Miocene. Evolutionary relationships within the genus, combined with limited spatial and temporal concordance among endemics, offer support for all three alternate models of diversification. Our findings emphasise the importance of peripherally isolated locations in creating and maintaining endemic species and their contribution to the biodiversity of the Indo-Australian Archipelago.

Biotic Interactions and the Future of Fishes on Coral Reefs: The Importance of Trait-Based Approaches.

Biotic interactions govern the structure and function of coral reef ecosystems. As environmental conditions change, reef-associated fish populations can persist by tracking their preferred niche or adapting to new conditions. Biotic interactions will affect how these responses proceed and whether they are successful. Yet, our understanding of these effects is currently limited. Ecological and evolutionary theories make explicit predictions about the effects of biotic interactions, but many remain untested. Here, we argue that large-scale functional trait datasets enable us to investigate how biotic interactions have shaped the assembly of contemporary reef fish communities and the evolution of species within them, thus improving our ability to predict future changes. Importantly, the effects of biotic interactions on these processes have occurred simultaneously within dynamic environments. Functional traits provide a means to integrate the effects of both ecological and evolutionary processes, as well as a way to overcome some of the challenges of studying biotic interactions. Moreover, functional trait data can enhance predictive modeling of future reef fish distributions and evolvability. We hope that our vision for an integrative approach, focused on quantifying functionally relevant traits and how they mediate biotic interactions in different environmental contexts, will catalyze new research on the future of reef fishes in a changing environment.

Anatomical basis of diverse jaw protrusion directionality in ponyfishes (Family Leiognathidae).

Protrusion of the oral jaws is a key morphological innovation that enhances feeding performance in fishes. The mechanisms of protrusion and the basis of variation in its magnitude are well studied, but little attention has been paid to the functional morphology of protrusion directionality, despite wide variation among teleost species from slightly dorsal to strongly ventral. Ponyfishes (Leiognathidae) comprise a group of 52 species that exhibit striking diversity in the directionality of jaw protrusion, providing a promising system for exploring its underlying basis in a single clade. We examined the anatomical basis of protrusion directionality by measuring eight traits associated with the size and positioning of oral jaw bones. Measurements were made on cleared and stained specimens of 20 ponyfish species, representing every major lineage within the family. Species fell into three nonoverlapping clusters with respect to directionality including dorsal, rostral, and ventral protruders. A key correlate of protrusion direction is the anterior-posterior position of the articular-quadrate jaw joint. As the joint position moves from a posterior to a more anterior location, the orientation of the relaxed mandible rotates from an almost horizontal resting position to an upright vertical posture. Abduction of the mandible from the horizontal position results in ventrally directed protrusion, while the more upright mandible rotates to a position that maintains dorsal orientation. The resting orientation of the premaxilla and maxilla, thus, vary consistently with protrusion direction. Mouth size, represented by length of the mandible and maxilla, is a second major axis of variation in ponyfishes that is independent of variation in protrusion directionality.

Do key innovations unlock diversification? A case-study on the morphological and ecological impact of pharyngognathy in acanthomorph fishes.

Key innovations may allow lineages access to new resources and facilitate the invasion of new adaptive zones, potentially influencing diversification patterns. Many studies have focused on the impact of key innovations on speciation rates, but far less is known about how they influence phenotypic rates and patterns of ecomorphological diversification. We use the repeated evolution of pharyngognathy within acanthomorph fishes, a commonly cited key innovation, as a case study to explore the predictions of key innovation theory. Specifically, we investigate whether transitions to pharyngognathy led to shifts in the rate of phenotypic evolution, as well as shifts and/or expansion in the occupation of morphological and dietary space, using a dataset of 8 morphological traits measured across 3,853 species of Acanthomorpha. Analyzing the 6 evolutionarily independent pharyngognathous clades together, we found no evidence to support pharyngognathy as a key innovation; however, comparisons between individual pharyngognathous lineages and their sister clades did reveal some consistent patterns. In morphospace, most pharyngognathous clades cluster in areas that correspond to deeper-bodied morphologies relative to their sister clades, whereas occupying greater areas in dietary space that reflects a more diversified diet. Additionally, both Cichlidae and Labridae exhibited higher univariate rates of phenotypic evolution compared with their closest relatives. However, few of these results were exceptional relative to our null models. Our results suggest that transitions to pharyngognathy may only be advantageous when combined with additional ecological or intrinsic factors, illustrating the importance of accounting for lineage-specific effects when testing key innovation hypotheses. Moreover, the challenges we experienced formulating informative comparisons, despite the ideal evolutionary scenario of multiple independent evolutionary origins of pharyngognathous clades, illustrates the complexities involved in quantifying the impact of key innovations. Given the issues of lineage specific effects and rate heterogeneity at macroevolutionary scales we observed, we suggest a reassessment of the expected impacts of key innovations may be warranted.