Untangling the relationship between developmental and evolutionary integration.

Patterns of integration and modularity among organismal traits are prevalent across the tree of life, and at multiple scales of biological organization. Over the past several decades, researchers have studied these patterns at the developmental, and evolutionary levels. While their work has identified the potential drivers of these patterns at different scales, there appears to be a lack of consensus on the relationship between developmental and evolutionary integration. Here, we review and summarize key studies and build a framework to describe the conceptual relationship between these patterns across organismal scales and illustrate how, and why some of these studies may have yielded seemingly conflicting outcomes. We find that among studies that analyze patterns of integration and modularity using morphological data, the lack of consensus may stem in part from the difficulty of fully disentangling the developmental and functional causes of integration. Nonetheless, in some empirical systems, patterns of evolutionary modularity have been found to coincide with expectations based on developmental processes, suggesting that in some circumstances, developmental modularity may translate to evolutionary modularity. We also advance an extension to Hallgrímsson et al.'s palimpsest model to describe how patterns of trait modularity may shift across different evolutionary scales. Finally, we also propose some directions for future research which will hopefully be useful for investigators interested in these issues.

Patterns of Phenotypic Evolution Associated with Marine/Freshwater Transitions in Fishes.

Evolutionary transitions between marine and freshwater ecosystems have occurred repeatedly throughout the phylogenetic history of fishes. The theory of ecological opportunity predicts that lineages that colonize species-poor regions will have greater potential for phenotypic diversification than lineages invading species-rich regions. Thus, transitions between marine and freshwaters may promote phenotypic diversification in trans-marine/freshwater fish clades. We used phylogenetic comparative methods to analyze body size data in nine major fish clades that have crossed the marine/freshwater boundary. We explored how habitat transitions, ecological opportunity, and community interactions influenced patterns of phenotypic diversity. Our analyses indicated that transitions between marine and freshwater habitats did not drive body size evolution, and there are few differences in body size between marine and freshwater lineages. We found that body size disparity in freshwater lineages is not correlated with the number of independent transitions to freshwaters. We found a positive correlation between body size disparity and overall species richness of a given area, and a negative correlation between body size disparity and diversity of closely related species. Our results indicate that the diversity of incumbent freshwater species does not restrict phenotypic diversification, but the diversity of closely related taxa can limit body size diversification. Ecological opportunity arising from colonization of novel habitats does not seem to have a major effect in the trajectory of body size evolution in trans-marine/freshwater clades. Moreover, competition with closely related taxa in freshwaters has a greater effect than competition with distantly related incumbent species.

Diversification along a benthic to pelagic gradient contributes to fish diversity in the world's largest lake (Lake Baikal, Russia).

Insights into the generation of diversity in both plants and animals have relied heavily on studying speciation in adaptive radiations. Russia's Lake Baikal has facilitated a putative adaptive radiation of cottid fishes (sculpins), some of which are highly specialized to inhabit novel niches created by the lake's unique geology and ecology. Here, we test evolutionary relationships and novel morphological adaptation in a piece of this radiation: the Baikal cottid genus, Cottocomephorus, a morphologically derived benthopelagic genus of three described species. We used a combination of mitochondrial DNA and restriction site associated DNA sequencing from all Cottocomephorus species. Analysis of mitochondrial cytochrome b haplotypes was only able to two resolve two lineages: C. grewingkii and C. comephoroides/inermis. Phylogenetic inference, principal component analysis, and faststructure of genome-wide SNPs uncovered three lineages within Cottocomephorus: C. comephoroides, C. inermis and C. grewingkii. We found recent divergence and admixture between C. comephoroides and C. inermis and deep divergence between these two species and C. grewingkii. Contrasting other fish radiations, we found no evidence of ancient hybridization among Cottocomephorus species. Digital morphology revealed highly derived pelagic phenotypes that reflect divergence by specialization to the benthopelagic niche in Cottocomephorus. Among Cottocomephorus species, we found evidence of ongoing adaptation to the pelagic zone. This pattern highlights the importance of speciation along a benthic-pelagic gradient seen in Cottocomephorus and across other adaptive fish radiations.

Patterns of Body Shape Diversity and Evolution in Intertidal and Subtidal Lineages of Combtooth Blennies (Blenniidae).

Marine intertidal zones can be harsher and more dynamic than bordering subtidal zones, with extreme and temporally variable turbulence, water velocity, salinity, temperature, and dissolved oxygen levels. Contrasting environmental conditions and ecological opportunities in subtidal versus intertidal habitats may generate differing patterns of morphological diversity. In this study we used phylogenetic comparative methods, measurements of body length, and two-dimensional landmarks to characterize body shape and size diversity in combtooth blennies (Ovalentaria: Blenniidae) and test for differences in morphological diversity between intertidal, subtidal, and supralittoral zones. We found that subtidal combtooth blennies have significantly higher body shape disparity and occupy a region of morphospace three times larger than intertidal lineages. The intertidal morphospace was almost entirely contained within the subtidal morphospace, showing that intertidal combtooth blennies did not evolve unique body shapes. We found no significant differences in body size disparity between tidal zones, no correlations between body shape and tidal zone or body size and tidal zone, and no body shape convergence associated with tidal zone. Our findings suggest that a subset of combtooth blenny body shapes are suitable for life in both subtidal and intertidal habitats. Many species in regions of morphospace unique to subtidal combtooth blennies exhibit distinct microhabitat use, which suggests subtidal environments promoted morphological diversification via evolutionary microhabitat transitions. In contrast, limited intertidal body shape diversity may be due to strong selective pressures that constrained body shape evolution and environmental filtering that prevented colonization of intertidal zones by certain subtidal body shapes.

Comparative morphology of shark pectoral fins.

Sharks vary greatly in morphology, physiology, and ecology. Differences in whole body shape, swimming style, and physiological parameters have previously been linked to varied habitat uses. Pectoral fin morphology has been used to taxonomically classify species and hypotheses on the functional differences in shape are noted throughout the literature; however, there are limited comparative datasets that quantify external and skeletal morphology. Further, fins were previously categorized into two discrete groups based on the amount of skeletal support present: (a) aplesodic, where less than half of the fin is supported and (b) plesodic where greater than half of the fin is supported. These discrete classifications have been used to phylogenetically place species, though the methodology of classification is infrequently described. In this study, we sampled fins from 18 species, 6 families, and 3 orders, which were also grouped into five ecomorphotype classifications. We examined the external morphology, extent of skeletal support, and cross-sectional shape of individual cartilaginous elements. Using phylogenetic comparative methods, we show that fin shape does not differ significantly between ecomorphotypes, suggesting there may be some mechanical constraint. However, we find that the internal anatomy of the fin does vary significantly between ecomorphotypes, especially the extent and distribution of calcification of skeletal support, suggesting that the superficial similarity of fin shapes across ecomorphotypes may belie differences in function. Finally, we find that a number of morphological variables such as number of radials, radial calcification and shape, and fin taper all correlate with the extent of skeletal support. Within these morphospaces, we also describe that some orders/families tend to occupy certain areas with limited overlap. While we demonstrate that there is some mechanical constraint limiting external variations in shark pectoral fin morphology, there are compounding differences in skeletal anatomy that occur within ecomorphotypes which we propose may affect function.

Addressing incomplete lineage sorting and paralogy in the inference of uncertain salmonid phylogenetic relationships.

Recent and continued progress in the scale and sophistication of phylogenetic research has yielded substantial advances in knowledge of the tree of life; however, segments of that tree remain unresolved and continue to produce contradicting or unstable results. These poorly resolved relationships may be the product of methodological shortcomings or of an evolutionary history that did not generate the signal traits needed for its eventual reconstruction. Relationships within the euteleost fish family Salmonidae have proven challenging to resolve in molecular phylogenetics studies in part due to ancestral autopolyploidy contributing to conflicting gene trees. We examine a sequence capture dataset from salmonids and use alternative strategies to accommodate the effects of gene tree conflict based on aspects of salmonid genome history and the multispecies coalescent. We investigate in detail three uncertain relationships: (1) subfamily branching, (2) monophyly of Coregonus and (3) placement of Parahucho. Coregoninae and Thymallinae are resolved as sister taxa, although conflicting topologies are found across analytical strategies. We find inconsistent and generally low support for the monophyly of Coregonus, including in results of analyses with the most extensive dataset and complex model. The most consistent placement of Parahucho is as sister lineage of Salmo.

2D or Not 2D? Testing the Utility of 2D Vs. 3D Landmark Data in Geometric Morphometrics of the Sculpin Subfamily Oligocottinae (Pisces; Cottoidea).

We contrast 2D vs. 3D landmark-based geometric morphometrics in the fish subfamily Oligocottinae by using 3D landmarks from CT-generated models and comparing the morphospace of the 3D landmarks to one based on 2D landmarks from images. The 2D and 3D shape variables capture common patterns across taxa, such that the pairwise Procrustes distances among taxa correspond and the trends captured by principal component analysis are similar in the xy plane. We use the two sets of landmarks to test several ecomorphological hypotheses from the literature. Both 2D and 3D data reject the hypothesis that head shape correlates significantly with the depth at which a species is commonly found. However, in taxa where shape variation in the z-axis is high, the 2D shape variables show sufficiently strong distortion to influence the outcome of the hypothesis tests regarding the relationship between mouth size and feeding ecology. Only the 3D data support previous studies which showed that large mouth sizes correlate positively with high percentages of elusive prey in the diet. When used to test for morphological divergence, 3D data show no evidence of divergence, while 2D data show that one clade of oligocottines has diverged from all others. This clade shows the greatest degree of z-axis body depth within Oligocottinae, and we conclude that the inability of the 2D approach to capture this lateral body depth causes the incongruence between 2D and 3D analyses. Anat Rec, 301:806-818, 2018. © 2017 Wiley Periodicals, Inc.

Littorally adaptive? Testing the link between habitat, morphology, and reproduction in the intertidal sculpin subfamily Oligocottinae (Pisces: Cottoidea).

While intertidal habitats are often productive, species-rich environments, they are also harsh and highly dynamic. Organisms that live in these habitats must possess morphological and physiological adaptations that enable them to do so. Intertidal fishes are generally small, often lack scales, and the diverse families represented in intertidal habitats often show convergence into a few general body shapes. However, few studies have quantified the relationship between phenotypes and intertidal living. Likewise, the diversity of reproductive traits and parental care in intertidal fishes has yet to be compared quantitatively with habitat. We examine the relationship of these characters in the sculpin subfamily Oligocottinae using a phylogenetic hypothesis, geometric morphometrics, and phylogenetic comparative methods to provide the first formal test of associations between fish phenotypes and reproductive characters with intertidal habitats. We show that the ability to live in intertidal habitats, particularly in tide pools, is likely a primitive state for Oligocottinae, with a single species that has secondarily come to occupy only subtidal habitats. Contrary to previous hypotheses, maximum size and presence of scales do not show a statistically significant correlation with depth. However, the maximum size for all species is generally small (250 mm or less) and all show a reduction in scales, as would be expected for an intertidal group. Also contrary to previous hypotheses, we show that copulation and associated characters are the ancestral condition in Oligocottinae, with copulation most likely being lost in a single lineage within the genus Artedius. Lastly, we show that body shape appears to be constrained among species with broader depth ranges, but lineages that occupy only a narrow range of intertidal habitats display novel body shapes, and this may be associated with habitat partitioning, particularly as it relates to the degree of wave exposure.

Molecular phylogenetics of sculpins of the subfamily Oligocottinae (Cottidae).

The sculpin subfamily Oligocottinae includes 18-20 species of nearshore benthic fishes with a diverse array of reproductive strategies. As a first step toward understanding the evolution of that diversity, we conducted a phylogenetic study based on DNA sequences from eight genomic regions from 31 sculpin species aimed at testing monophyly and relationships of the Oligocottinae. Representatives from the perciform families Agonidae, Cottidae, Hemitripteridae, Hexagrammidae, Psychrolutidae, and Rhamphocottidae served as outgroups. The sequence data were analyzed in maximum likelihood and Bayesian phylogenetic inference frameworks. Results of these analyses show that a systematic revision of the group is warranted. The genus Clinocottus is a polyphyletic assemblage of three distinct lineages, which should be indicated by resurrection of the subgenera Blennicottus, Clinocottus, and Oxycottus; Leiocottus hirundo is more closely related to Clinocottus analis than C. analis is related to any other member of Clinocottus; the composition of the tribe Oligocottini should be revised to include only the genera Oligocottus, Clinocottus, and Orthonopias; and the genus Sigmistes should be removed from the subfamily Oligocottinae.