New Paper on Cichlids: The ecological and genomic basis of explosive adaptive radiation

I am pleased to announce a new paper I have co-authored with a number of colleagues from Africa, Australia, Europe, and the United States investigating the ecological and genomic basis of adaptive radiation in cichlids. Adaptive radiations are the rapid speciation and ecological divergence from a common ancestor. Well known examples include things such as Darwin’s finches, Hawaiian silverswords, and Caribbean anoles. Cichlids are famous for undergoing adaptive radiations in a number of lakes (such as Lake Tanganyika, Lake Nicaragua, Lake Malawi, and Lake Victoria) as well as at the continental scale. Because of this, cichlids are often used as a model to study various biological aspects of adaptive radiation. In this paper, we investigate what parts of the cichlid tree of life have the fastest rates of speciation and also tested a number of previously proposed biotic (male ornamentation, polygamy, etc.) and abiotic (rainfall, temperature) factors that have been proposed for the staggering diversity.

We built an evolutionary tree of all cichlids and calculated speication rates. We found the fastest rates of speciation in cichlids occur in Lake Victoria, an extremely young lake (some estimates as young as 15,000 years) in East Africa that contains several hundred species. The speciation rate is one of the fastest observed in contemporary animals! Lake Malawi and Lake Nicaragua also possess fast rates. While regression and non-parametric analyses found male ornamentation and water depth to be positively linked to speciation while arid climates and non-cichlid predatory fish lineages were found to negatively effect speciation, but these had weak explanatory power . However when fitting more complex hidden-state models that allow for accounting for rates to be influenced by unobserved states (think of this as a more complex null model), we find that none of these factors actually explains the observed diversification patterns.

Phylogeny of all cichlids with branches showing hot spots in speciation rate. Cooler colors represent slower rates while warmer colors represent faster rates. Speciation rates are shown in b, where cichlids in Lake Victoria have the fastest rates, followed by those in Lake Malawi, other East African Lakes containing the Lake Victoria cichlid superflock and crater lakes, such as Lake Nicaragua and Lake Barombi Mbo (Cameroon). c shows the effect of various biotic and abiotic factors on speciation rates.

Because we found no traits responsible for the explosive radiation of cichlids, we examined the genomic substrate of adaptive radiation by comparing species pairs from a number of cichlid adaptive radiations. We found that speciation rates in these radiations was highly correlated with the number of divergently fixed indels (insertions or deletions of DNA bases in a genome )relative to the age of the radiation. For example, Lake Victoria, which has fast speciation rates and is young had the greatest number of divergently fixed indels. We then did a more in depth genomic analysis of 100 Lake Victorian cichlid species genomes. We find that the cichlids of Lake Victoria share are a hybrid swarm and that there are many indels that segregate between Lake Victorian cichlid species. While some of these were found only in Lake Victoria cichlids, a large number of the indels that segregate between Lake Victorian cichlids were also found in cichlids found outside the radiation and that Lake Victorian cichlids contain variants that existed up to 10 million years before the Lake Victoria adaptive radiation started (remember the Lake Victoria cichlid radiation is quite young, ~15,000 years old). Interestingly, these indels were often found to be associated with various dimensions of ecological diversity, such as traits associated with diet and habitat use, much more so than indels found in only Lake Victorian cichlids. This highlights that the genomic potential of the radiation was in place long before it formed, providing the genomic architecture of the radiation and that recombination of genomic elements through hybridization provided genomic diversity that allowed for the rapid diversification of the radiation.

Network of Lake Victorian cichlids. Lines between species represent shared genomic blocks between species. The shape around species represents the habitat type they occupy while the color represents their diet. Species that live in similar habitats and have similar diets tend to share more genomic blocks.

Paper Citation and Link: McGee MD, Borstein SR, Meier JI, Marques DA, Mwaiko S, Taabu A, Kishe-Machumu MA, O’Meara BC, Bruggmann R, Excoffier L, and Seehausen O. 2020. The ecological and genomic basis of explosive adaptive radiation. 10.1038/s41586-020-2652-7

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New Paper on the Metabolomics of Narrowleaf Cottonwoods

I am happy to announce that in collaboration with ecologists and chemists at the University of Tennessee, that we have published a paper investigating the metabolomics of Narrowleaf Cottonwood trees (Populus angustifolia) across the Southwestern United States. The paper discusses using Ultra-Performance Liquid Chromatography–High-Resolution Mass Spectrometry to assess the molecular profile of Narrowleaf Cottonwoods clones from six populations grown in a common garden. We found that these populations had distinct metabolomes, that is molecular compounds (such as proteins, lipids, carbohydrates, etc.) and that population itself explains about 36% of the differences in associated chemical compounds found in the soil around the roots of these plants. This suggests that different populations condition the soil around them in different ways, which is important in understanding plant-soil interactions that may be important for species divergence, the success of invasive species colonizing, and plant community succession.

Indicator Compounds for the soul and roots of six Narrowleaf Cottonwood populations. These are Van Krevelen diagrams that show differences in the oxygen (O) to carbon (C) and hydrogen (H) to carbon (C) ratios. Boxes inside plots represent different chemical classes (e.g. lipids). Green points represent significant indicator compounds that differentiate populations from each other.

Paper Citation and Link: Mueller LO, Borstein SR, Tague ED, Dearth SP, Castro HF, Campagna SR, Bailey JK, and Schweitzer JA. 2020. Populations of Populus angustifolia have evolved distinct metabolic profiles that influence their surrounding soil. Plant and Soil 448:399-411. 10.1007/s11104-019-04405-2

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Release of a New R Package, dietr to Calculate Trophic Indices

I am excited to announce the release of a new R package I have worked on, dietr (Diet Estimated Trophic Levels), which can be used to estimate a number of indices used in the study of trophic ecology, such as trophic levels, electivity indices, and compound diet indices. dietr is maintained on GitHub and available for R via a download from CRAN. A paper describing dietr is currently in review, but a detailed tutorial on using the package is availble via the vignette feature in R.

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Seminar Talk 2/21/19 @ University of Tennessee

I will be giving a lightning talk on February 21, 2019 at the University of Tennessee about my research on the role of pharyngeal jaws in acanthomorph fish diversity. The talk will occur at 3:30 in the 307 SERF (Science & Engineering Building) on the University of Tennessee, Knoxville campus.

PJAsize

Specialized pharyngeal jaws are found in six families of fish, including the cichlids. Above is a distribution of size-corrected (for body size) diameter of the pharyngeal gape.

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AnnotationBustR Paper Published in PeerJ

I’m happy to announce that the paper describing the R package AnnotationBustR Brian O’Meara and I created has been accepted at PeerJ. This package extracts subsequences from GenBank Annotations. For more details about the R package, check out the previous blog-post: AnnotationBustR, a New R Package and Pre-Print That Extracts Sequence Data From GenBank Annotations.

Paper Citation and Link: Borstein SR, O’Meara BC. (2018AnnotationBustR: an R package to extract subsequences from GenBank annotationsPeerJ 6:e5179.
https://doi.org/10.7717/peerj.5179

For a link to the R package on CRAN: https://cran.r-project.org/web/packages/AnnotationBustR/index.html

GitHub Development Repo: https://github.com/sborstein/AnnotationBustR

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New Paper on Cichlid Feeding Kinematic Efficiency Published in Evolution

A paper I collaborated on with Christopher Martinez on Malawi and Tanganyikan cichlid kinematics was recently published in Evolution. This paper builds upon a kinematic dataset and paper I worked on that you can find more information about on my site here. Most fish (including cichlids) can be categorized as either suction feeders or biters. Suction feeders by protruding their jaws, depressing their hyoid bone, and abducting the operculum (gill plate) generate a suction force to suck their prey into their mouth. Biters directly contact and forcefully remove the prey with their jaws.

In this paper, we track how the feeding apparatus changes during a feeding event mapping its morphology (see below photo) and investigated how it relates to exploiting functionally different prey. The linearity of the mapped trajectory can then be used to assess how efficient the strike is, with a more linear strike being more efficient.

2018 Cichlid Kinematic Efficiency.pdf - Adobe Acrobat Pro DC1

The above depicts how the craniofacial (head and face) morphology of Lamprologus lemairii, a fish and crustacean predator that employs suction feeding to capture prey, changes throughout prey capture. The figure shows how we tracked kinesis and the overall trajectory as the head moves from the beginning (teal dot) of a feeding event to the maximum expansion of the jaws during a feeding event (red dot). Light blue dots are individual morphological landmarks tracked throughout the strike while the yellow dots are along a curve tracked throughout the strike. Dark blue dots and associated photos show how these landmarks move at roughly evenly spaced out intervals throughout the strike. The dotted line depicts the overall kinematic trajectory.

We find that fish that feed on evasive prey items, fish that typically employ suction feeding to capture prey, have more cranial kinesis during a strike, as the jaws protrude to aid in generating suction force (see the below photo). While the jaws and other aspects of the head do undergo a vast amount of kinesis during feeding, we find that they have much more kinematically efficient (i.e. more linear) than species that employ biting (algae, sponge, mollusk feeders, etc.) and have far less jaw kinesis. Our study highlights underappreciated aspect of jaw protrusion, how it aids in kinematic efficiency, which may help in understanding the origins and diversity of jaw morphology in ray-finned fishes.

2018 Cichlid Kinematic Efficiency.pdf - Adobe Acrobat Pro DC

Phylogeny of Lake Malawi and Tanganyikan cichlids depicting the diet of species, the amount of cranial kinesis, and with representative photos showing how morphology changes during feeding. Branch colors of the phylogeny depict the amount of cranial kinesis, with species on cooler colored branches having more cranial kinesis and species on warmer colored branches having less cranial kinesis. Colored dots next to species names represent one of the six diet classifications used to categorize species (i.e. fish, zoobenthos, aufwuchs, etc.). From the various pictures of fish heads, it is easy to see that species that feed on more evasive prey items (fish, zoobenthos 2 (which includes shrimps) have more cranial kinesis than species that employ biting to feed on non-evasive prey items (aufwuchs, zoobenthos 1 (which includes snails and bivalves).

The citation and link to the paper:

Martinez CM, McGee MD, Borstein SR, and Wainwright PC. 2018. Feeding ecology underlies the evolution of cichlid jaw mobility. Evolution.
 https://doi.org/10.1111/evo.13518.

 

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AnnotationBustR, a New R Package and Pre-Print That Extracts Sequence Data From GenBank Annotations

I have recently published a new R package, AnnotationBustR, and a Preprint of our paper that is submitted at PeerJ. Sequence data can be difficult to work with sometimes as sequences may be concatenated or a sequence of interest may be in a genome and not available by itself on GenBank. Additionally, the same gene may be annotated may be annotated differently among records,  making it difficult to extract data from a lot of records. AnnotationBustR was written to make this process easier and as users can supply a list of accessions and a set of terms they want to extract and get FASTA formatted files returned. We provide a vignette tutorial within the R package or on CRAN (see link below) on how to use the software.

The R package is developed on GitHub and  interfaces to GenBank through the R package seqinr. You can see the GitHub repo, CRAN page, and pre-print of our paper in the links below:

GitHub: https://github.com/sborstein/AnnotationBustR

CRAN: https://cran.r-project.org/web/packages/AnnotationBustR/index.html

PeerJ Preprint citation and link: Borstein, S. R., & O’Meara, B. C. (2017). AnnotationBustR: An R package to extract subsequences from GenBank annotations. PeerJ Preprints, e2920v1, https://doi.org/10.7287/peerj.preprints.2920v1.

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I’ve Been Awarded an NSF DDIG!

I have been awarded a National Science Foundation Doctoral Dissertation Improvement Grant for my research on the morphological consequences of trophic evolution. I look forward to providing information on the research products produced by this funding on this site in the future. A brief summary of my project can be found here: https://www.nsf.gov/awardsearch/showAward?AWD_ID=1701913&HistoricalAwards=false

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Presentation at SICB 2017 New Orleans, LA

I will be presenting a talk at this years Society of Integrative and Comparative Biologists annual meeting January 7th, 2017 in New Orleans. The talk “The evolution of diet breadth in coral reef fishes” will discuss how diet breadth effects phenotypic evolution in reef fishes. The talk is in the convention center room 217 at 11:15 AM.

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New Paper in Proceedings of the Royal Society B on Biting and Suction Feeding in Rift Lake Cichlids

I’m happy to announce a paper I collaborated on investigating how feeding modes effect jaw kinesis in cichlids was recently published in Proceedings of the Royal Society B: Biological Sciences.

In this paper we used a combination of ultra-conserved element sequencing (UCE) and high-speed video to investigate if the mode at which fish procure their food effects the evolution of jaw protrusion in Lake Malawi and Tanganyikan fishes. A distinctive feature of ray-finned fishes (which include cichlids) is that many of them are able to protrude the upper jaw when feeding. This jaw protrusion is especially useful when feeding on evasive prey items as it enhances the suction force and aides in sucking the prey into the mouth. For the most part, fish feed by two methods. Suction feeding, where prey is obtained by the method described above or biting, where prey is forcefully removed/captured by the jaws themselves (e.x. fish feeding of algae/sponged off rocks, scale eaters, mollusk shellers).

2016 Cichlid replicated divergence mirrors ver.pdf - Adobe Acrobat Pro DC

Lamprologus lemairii, a fish and crustacean predator that employs suction feeding, showing how the jaw bones protrude during feeding. The above photo shows the position of the bones before a strike while the bottom shows where the same points have moved to once prey is captured.

Our results showed that species that obtain prey via biting have much less jaw protrusion and overall movement of the cranial bones during a feeding event relative to suction feeders. This is not necessarily surprising as biting fish face certain functional demands on the jaws, like stress placed by forcible contact to extract prey, where additional jaw protrusion would be ineffective. Our results highlight  the contrasting functional demands and trade-offs both modes of feeding have and how these demands have shaped the evolution of head morphology and feeding ecology in the Malawi and Tanganyikan cichlid radiations.

Kinesis

A phylogeny constructed from ultra-conserved elements of 56 Malawi and Tanganyikan cichlids used in the study. Feeding mode has transitioned numerous times through the evolution of these fishes as can be seen by the different colors of the branches of the phylogeny, with biting species highlighted in warmer colors and suction feeding species by cooler colors.

Paper Citation & Link : McGee MD, Faircloth BC, Borstein SR, Zheng J, Hulsey CD, Wainwright PC, and Alfaro ME. 2016. Replicated divergence in cichlid radiations mirrors a major vertebrate innovation. Proceedings of the Royal Society B: Biological Sciences 283. http://dx.doi.org/10.1098/rspb.2015.1413

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