Littorally adaptive? Testing the link between habitat, morphology, and reproduction in the intertidal sculpin subfamily Oligocottinae (Pisces: Cottoidea)
- Published
- Accepted
- Subject Areas
- Evolutionary Studies, Marine Biology, Zoology
- Keywords
- evolution, fishes, geometric morphometrics, body shape, reproduction, intertidal, phylogenetic comparative methods
- Copyright
- © 2017 Buser et al.
- Licence
- This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ Preprints) and either DOI or URL of the article must be cited.
- Cite this article
- 2017. Littorally adaptive? Testing the link between habitat, morphology, and reproduction in the intertidal sculpin subfamily Oligocottinae (Pisces: Cottoidea) PeerJ Preprints 5:e2981v1 https://doi.org/10.7287/peerj.preprints.2981v1
Abstract
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 (250mm 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.
Author Comment
This is a submission to PeerJ for review.
Supplemental Information
Ancestral state reconstruction of tide pool occupancy for the sculpin subfamily Oligocottinae and the outgroup taxon Chitonotus pugetensis
The most recent common ancestor (MRCA) of Oligocottinae and the MRCA of the Leiocottus lineage are each indicated with an arrow. See text for details.
Phenogram showing the inferred evolutionary history of maximum length of extant oligocottine species and the outgroup taxon Chitonotus pugetensis
The most recent common ancestor (MRCA) of Oligocottinae is indicated with an arrow. Phylogenetic relationships are represented by white edges and bifurcation points represent inferred speciation events. Phylogenetic topology is from Bayesian MCC tree shown in Figure 1. Relative time is indicated on the horizontal axis and maximum length in millimeters indicated on the vertical axis. The tips and nodes of the phylogeny are positioned on the vertical axis to reflect the maximum length or inferred maximum length of each taxon or hypothetical ancestor (respectively). Ancestral states for each node were inferred using maximum likelihood and 95% confidence intervals for each state are represented with blue lines. See text for details.
Ancestral state reconstruction of the presence of squamation for the sculpin subfamily Oligocottinae and the outgroup taxon Chitonotus pugetensis
The most recent common ancestor (MRCA) of Oligocottinae, the MRCA of the subgenus Clinocottus (Blennicottus), and the MRCA of the clade composed of Oligocottus snyderi, O. rubellio, and O. maculosus are each indicated with an arrow. See text for details.
Ancestral state reconstruction of the presence of copulation for the sculpin subfamily Oligocottinae and the outgroup taxon Chitonotus pugetensis
The most recent common ancestor (MRCA) of Oligocottinae is indicated with an arrow. Tips and nodes without a pie symbol are taxa for which no data are available or the state is not reconstructable due to missing data (respectively). See text for details.
Morphospace of significant principal component axes showing inferred phenotypic optima for the sculpin subfamily Oligocottinae and the outgroup taxon Chitonotus pugetensis
Taxa (small circles, labeled by species name) are color-coded to match their inferred phenotypic optimum (large circles). Optima inferred using “surface” (Ingram & Mahler, 2013). See text for details.
Reference:
Ingram T., Mahler DL. 2013. SURFACE: detecting convergent evolution from comparative data by fitting Ornstein-Uhlenbeck models with stepwise Akaike Information Criterion. Methods in Ecology and Evolution 4:416–425.
Morphological variation in enlarged male genital papillae
Species and museum lot numbers are as follows, A) Artedius harringtoni, OSIC 04533, 91mm SL; B) Clinocottus acuticeps, UAM 47713, 30mm SL; C) Oligocottus maculosus, OSU 07467, 73mm SL; D) Chitonotus pugetensis, OSU 14872, 76mm SL; E) Clinocottus analis, OSU 3241, 72mm SL; F) Clinocottus globiceps, OSU 00275, 104mm SL. Lot numbers begin with a three letter code which indicates the location of the specimen: OSU = Oregon State University, UAM = University of Alaska Museum. Scale bar = 2mm.
Modification of the anteriormost rays of the anal in males of the genus Oligocottus
Illustration of anal fin is shown for all species: A) O. rimensis, SIO 67-151; B) O. maculosus, OS 287; C) O. rubellio, OS 8133; D) O. snyderi, OS 4366. Cladogram indicating phylogenetic relationship of species is indicated below anal fin illustrations, adapted from Figure 3. Museum codes are SIO = Scripps Institute of Oceanography, OS = Oregon State University.
GenBank accession numbers for all sequences used in this study from the dataset assembled in Buser and Lopez (2015)
Comma separated values (CSV) format. See Buser and Lopez (2015) for collection locality data and DNA isolation and amplification methodology.
GenBank accession numbers for all sequences used in this study from the dataset assembled in Buser and Lopez (2015)
Microsoft Excel (xlsx) format. See Buser and Lopez (2015) for collection locality data and DNA isolation and amplification methodology.
Museum collection data for all 16 species of the subfamily Oligocottinae and the outgroup taxon Chitonotus pugetensis
Comma seperated values (CSV) format.
Museum collection data for all 16 species of the subfamily Oligocottinae and the outgroup taxon Chitonotus pugetensis
Microsoft Excel (xlsx) format. Museum records where "tide pool" or the like is explicitly stated as the collection locality are highlighted in light green.
Verbatim descriptions of depth ranges for members of the sculpin subfamily Oligocottinae (ingroup) and the outgroup taxon Chitonotus pugetensis
Microsoft Excel (xlsx) format. Verbatim descriptions of depth ranges, primary literature references for tide pool occurrence, and museum lots where "tide pool" or the like is listed as the collection locality. List of museum codes and references are below the table.
Verbatim descriptions of depth ranges for members of the sculpin subfamily Oligocottinae (ingroup) and the outgroup taxon Chitonotus pugetensis
Comma separated values (csv) format. Verbatim descriptions of depth ranges, primary literature references for tidepool occurrance, and museum lots where "tide pool" or the like is listed as the collection locality. List of museum codes and references are below the table.
Summary of collection depth data for museum records of oligocottine sculpins and the outgroup taxon Chitonotus pugetensis
Microsoft Excel (xlsx) format. Catalog numbers, depth, and locality data are provided in Supplementary Table 2.
Summary of collection depth data for museum records of oligocottine sculpins and the outgroup taxon Chitonotus pugetensis
Comma separated values (csv) format. Catalog numbers, depth, and locality data are provided in Supplementary Table 2.
Folder containing R script, data matrix, shape data, and phylogenetic tree
The R script is titled "LitorallyAdaptiveScript.R" and contains a heavily annotated list of commands for importing the data matrix ("LitorallyAdaptive_datamatrix.csv"), shape data ("MorphoJcoords.csv"), and phylogenetic tree ("sculpin_birthdeath_mcc_starbeast.tree"), and performing all R-based analyses described in the manuscript. The script also contains descriptions of data contained in each file.