Variation of tooth traits in ecologically specialized and sympatric morphs

Guðbjörg Ósk Jónsdóttir*, Finnur Ingimarsson, Sigurður Sveinn Snorrason, Sarah Elizabeth Steele, Arnar Pálsson. Submitted to Evolutionary Biology.

GOJ: https://orcid.org/0009-0008-0502-5553
FI: https://orcid.org/0000-0002-0815-7622
SES: https://orcid.org/0000-0001-8404-5537
AP: https://orcid.org/0000-0002-6525-8112

Rotational from top left, premaxilla, maxilla, supramaxilla  (w.o. teeth) and palatine.

Abstract
Differences in dentition between species relate to feeding specialisations, as examples of tetrapod dentition variation show clearly. The association of tooth traits and specialisations in non-mammalian vertebrates is less studied. We examined variation in dental traits in four sympatric morphs of Arctic charr (Salvelinus alpinus) which differ in feeding specialisations, head and jaw bone morphology. We studied tooth numbers in six bones (dentary, maxilla, premaxilla, palatine, vomer and glossohyal) and tooth angles in one bone (maxilla). We found fluctuating asymmetry in tooth numbers and angles and that the allometry of tooth numbers varied by bone but not morphs. The tooth numbers differed by morphs in four bones (dentary, palatine, vomer and glossohyal). In general, the morphs defined as pelagic had more teeth, and this relates partially to changes in bone shape. There was a difference in maxilla tooth angle, with benthic morphs having teeth which were angled more inwards. Dentary and maxilla tooth number correlated moderately with bone shape, maxilla tooth angle and premaxilla tooth number did not. While it is currently unknown what tooth characteristics are ancestral vs derived in these populations, the marked differences in specific bones presents an opportunity to explore rapid adaptive evolution in dentition.

Large benthic charr on the spawning grounds, picture took Kalina H. Kapralova and Quentin Horta.

Now published in the Icelandic Naturalist. Areas used by Salmonid juveniles in Lake Þingvallavatn and connected rivers. Uppeldissvæði laxfiska í Þingvallavatni og tengdum ám (in icelandic, w. English abstract). Guðbjörg Ósk Jónsdóttir, Benóný Jónsson, Magnús Jóhannsson og Arnar Pálsson.  (Náttúrufræðingurinn).

Nursery grounds of juvenile fish provide them shelter and food making them essential for the life of an individual, the population and species as a whole. In Lake Þingvallavatn, Iceland, two species of salmonids inhabit the lake, Brown trout (Salmo trutta) and Arctic charr (Salvelinus alpinus). Extensive biological studies have been conducted on adult fish of both species in the lake and its catchment area, but much less is known about the biology of age-0 fish and the ecology of their first 1−2 years in the life. Given the critical importance of nursery areas for the existence of fish populations and their contribution to biological diversity, research was undertaken to examine the distribution of charr and trout juveniles in the surf zone of Lake Þingvallavatn and in streams connected to the lake. The research questions were,

1) Where in the lake and connected streams are juvenile fish found?

2) Has the density of charr and trout juveniles changed in the last twenty years?

3) Is there a connection between the environmental conditions and the presence of juvenile fish?

Data from Veiðimálastofnun (now Hafrannsóknastofun) surveys of salmonid juveniles in Þingvallavatn and adjacent rivers, spanning 2000 to 2021, were analyzed. In the summer of 2022, ten locations in Þingvallavatn were surveyed, fish were caught and measured, and several environmental factors were assessed using electrofishing. Fish were counted, identified by species, and measured for length and weight. Additionally, environmental factors, including the lake bottom composition and shoreline vegetation, were documented. The results show that the two species utilize different juvenile habitats, trout predominantly occupy river habitats, whereas charr are more abundant in the surf zone of the lake. There was a significant increase in density of the Brown trout over the 19-year period, but density of Arctic charr remained relatively stable with a sign of subtle decline. In 2022, six possible nursery sites were documented in the surf zone, four with majority of Arctic charr and two with mainly Brown trout. There was little overlap in the species distribution. Vegetation on the shoreline was the only environmental factor significantly correlated with the presence or absence of juvenile fish on a given site. Further studies on juvenile fish biology in the lake and adjacent streams and river might explore the interplay of environmental factors and genetics in shaping the size and morphology of adult fish in both species´ populations. This is particularly relevant for Arctic charr, which features four distinct sub-populations (or morphs) differing in size, shape, trophic morphology and ecology.

In January 2023 I was asked to give a historical account of the discovery of DNA helix in a local medical conference. From that I wrote a little piece about the discovery and discussed how DNA is seriously overinterpreted in modern society, as synonymous with Fate and a determinant stronger than environmental factors.

Sorry, no translation available.

Guðbjörg´s first paper is now published in PLoS-One.

Jónsdóttir GÓ, von Elm L-M, Ingimarsson F, Tersigni S, Snorrason SS, Pálsson A, et al. (2024) Diversity in the internal functional feeding elements of sympatric morphs of Arctic charr (Salvelinus alpinus). PLoS ONE 19(5): e0300359.

Abstract

The diversity of functional feeding anatomy is particularly impressive in fishes and correlates with various interspecific ecological specializations. Intraspecific polymorphism can manifest in divergent feeding morphology and ecology, often along a benthic–pelagic axis. Arctic charr (Salvelinus alpinus) is a freshwater salmonid known for morphological variation and sympatric polymorphism and in Lake Þingvallavatn, Iceland, four morphs of charr coexist that differ in preferred prey, behaviour, habitat use, and external feeding morphology. We studied variation in six upper and lower jaw bones in adults of these four morphs using geometric morphometrics and univariate statistics. We tested for allometric differences in bone size and shape among morphs, morph effects on bone size and shape, and divergence along the benthic-pelagic axis. We also examined the degree of integration between bone pairs. We found differences in bone size between pelagic and benthic morphs for two bones (dentary and premaxilla). There was clear bone shape divergence along a benthic–pelagic axis in four bones (dentary, articular-angular, premaxilla and maxilla), as well as allometric shape differences between morphs in the dentary. Notably for the dentary, morph explained more shape variation than bone size. Comparatively, benthic morphs possess a compact and taller dentary, with shorter dentary palate, consistent with visible (but less prominent) differences in external morphology. As these morphs emerged in the last 10,000 years, these results indicate rapid functional evolution of specific feeding structures in arctic charr. This sets the stage for studies of the genetics and development of rapid and parallel craniofacial evolution.

Wonderful for Guðbjörg and Sarah who made this such a stellar paper, with amazing visuals. For me it feels good to publish in PLoS One again, 10 years after my favorite paper on Eve and Hunchback (Naturally Occurring Deletions of Hunchback Binding Sites in the Even-Skipped Stripe 3+7 Enhancer. 2014. Palsson A, Wesolowska N, Reynisdóttir S, Ludwig MZ, Kreitman M. PLoS ONE 9(5): e91924. doi:10.1371/journal.pone.0091924.)

The prey availability and diet of juvenile Atlantic salmon (Salmo salar L.) in low-productivity rivers in northern Europe

accepted for publication in the Journal of Fish Biology. http://doi.org/10.1111/jfb.15757 

Authors:

Sum Yi Lai^1,2,  Arnar Pálsson², Guðni Guðbergsson¹, Ingi Rúnar Jónsson¹, Jón S. Ólafsson¹, Hlynur Bárðarson¹

1. Marine and Freshwater Research Institute, Hafnarfjördur, Iceland

2. University of Iceland, Reykjavík, Iceland

Corresponding author: Name: Sum Yi Lai Address: Marine and Freshwater Research Institute, Fornubúdir 5, 220 Hafnarfjördur, Iceland,

Email: sammi.lai@hafogvatn.is

Abstract:

The availability of resources varies across a species distributional range, and a low productivity area can make a species more vulnerable. We investigated the invertebrate composition and prey choice of juvenile Atlantic salmon (Salmo salar L.) in low productivity rivers at Northeast Iceland, which is one of the species´ most northerly distributions. By sampling benthic and drift invertebrate populations, we found that prey availability was similar within and between rivers. Gut content samples showed that the main prey choice for juvenile S. salar was the Chironomidae. The type of food items consumed varied across different weight groups of S. salar, with smaller juveniles having more diverse diet. S. salar did not have a selection preference for chironomids, which indicate that they were eating the highly available prey in their environment, rather than hunting high biomass items such as terrestrial invertebrates and large Dipterans. Estimates of dietary niche showed that S. salar in these low-productivity rivers relied on consuming what was most readily available, the chironomids, and that they must share resources with other salmonid species. This may be due to the low diversity of freshwater invertebrates (fewer prey options), whereas S. salar in nutrient-rich rivers could rely more on terrestrial invertebrates as an additional subsidy in their diet. In conclusion, with limited prey choices, juvenile S. salar in nutrient-poor rivers, especially in a biogeographically isolated region with low species diversity, may increase in vulnerability and decrease in adaptability to environmental change. Management methods that increase benthic prey abundance and diversity are recommended for conserving S. salar population in a nutrient-poor river

Log10 average number of prey items found in stomachs of juvenile Atlantic salmon (Salmo salar) was differed significantly across rivers (p<0.001) and by weight ranges (p<0.001).
The number of prey items consumed increased with weight (p<0.05). Log10 abundance also varies between taxonomic groups for all rivers (p<0.001) with abundances of Chironomidae higher in comparison.

It was at the Drosophila meeting in San Diego 10-14th of April 2002. I had arrived with my uncle Einar Arnason and his late wife Betty, after driving down from Passadena. In the ginormous reception ball room we snacked and drank, until Einar was bundled by a springly fellow with wired hair and manners. Marty Kreitman had arrived at the scene.

Drosophila Research Conference (drosophila-conf.org)

I had greatly admired his population genetic work, though it was the work Marty did with Misha Ludwig that particularly impressed me. The first did population genetics on the best characterized regulatory element at the time, the stripe 2 enhancer of the eve (even-skipped) gene of D. melanogaster, and then moved to functional studies, comparing the element between species. See for instance a very impressive paper on chimeras of D. melanogaster and D. pseudoobscura s2e enhancers.

Evidence for stabilizing selection in a eukaryotic enhancer element.

To make a long story short, serendipity helped me make Marty´s acquaintance and a year later I started a postdoc with him and Misha at the University of Chicago. There we had three fun years doing population genetics on enhancers and analyzing gene expression in embryos.

Functional evolution of a cis-regulatory module. 2005. Ludwig MZ, Palsson A, Alekseeva E, Bergman CM, Nathan J, Kreitman M. PLoS Biology. 3(4):e93. (doi:10.1371/journal.pbio.0030093 PDF)

Canalization of segmentation and its evolution in Drosophila. 2007. Lott SE, Kreitman M, Palsson A, Alekseeva E, Ludwig MZ. Proc Natl Acad Sci U S A. 104(26):10926-31. (doi: 10.1073/pnas.0701359104 PDF)

Naturally Occurring Deletions of Hunchback Binding Sites in the Even-Skipped Stripe 3+7 Enhancer. 2014. Palsson A, Wesolowska N, Reynisdóttir S, Ludwig MZ, Kreitman M. PLoS ONE 9(5): e91924. doi:10.1371/journal.pone.0091924.

In the summer of 2022 former trainees and friends of Marty arranged a nice farewell symposium for him in Chicago. Thankfully I got to participate via zoom, and see some of the great people again.

The manuscript got quite favorable replies.

https://www.biorxiv.org/content/10.1101/2023.02.17.528955v2 

We are continuing uploading the figures to Figshare+ and code to Github.

And adjusting the figures with new colour-blind friendlier palette.

See for instance.

"Dear Dr Dellinger

I am pleased to inform you that your manuscript RSPB-2023-2302 entitled "Variation in personality shaped by evolutionary history, genotype, and developmental plasticity in response to feeding modalities in the Arctic charr" has been accepted for publication in Proceedings B."

Dellinger, Marion; Steele, Sarah; Sprockel, Evert; Philip, Joris; Pálsson, Arnar; Benhaïm, David.

Very welcome outcome. Congrats to Sarah Steele and Marion Dellinger who led the study.

Boldness in behavior varied substantially by morphs, and also by families in some of the morphs, though noticably least in Anadromous (left) and planktivorous charr from Þingvallavatn (right).

Boldness variation by families of 5 Arctic charr ecomorphs

Submission of Guðbjörgs manuscript to PLoS One, second version of M.S. available on bioRxiv.

Diversity in the internal functional feeding elements of sympatric morphs of Arctic charr (Salvelinus alpinus)

Guðbjörg Ósk Jónsdóttir, Laura-Marie von Elm, Finnur Ingimarsson, Samuel Tersigni, Sigurdur Sveinn Snorrason, Arnar Palsson, Sarah Elizabeth Steele

The diversity of functional feeding anatomy is particularly impressive in fishes and correlates with various interspecific ecological specializations. Intraspecific polymorphism can manifest in divergent feeding morphology and ecology, often along a benthic pelagic axis. Arctic charr (Salvelinus alpinus) is a freshwater salmonid known for morphological variation and sympatric polymorphism and in Lake Þingvallavatn, Iceland, four morphs of charr coexist that differ in preferred prey, behaviour, habitat use, and external feeding morphology. We studied variation in six upper and lower jaw bones in adults of these four morphs using geometric morphometrics and univariate statistics. We tested for allometric differences in bone size and shape among morphs, morph effects on bone size and shape, and divergence along the benthic-pelagic axis. We also examined the degree of integration between bone pairs. We found differences in bone size between pelagic and benthic morphs for two bones (dentary and premaxilla). There was clear bone shape divergence along a benthic pelagic axis in four bones (dentary, articular angular, premaxilla and maxilla), as well as allometric shape differences between morphs in the dentary. Notably for the dentary, morph explained more shape variation than bone size. Comparatively, benthic morphs possess a compact and taller dentary, with shorter dentary palate, consistent with visible (but less prominent) differences in external morphology. As these morphs emerged in the last 10,000 years, these results indicate rapid functional evolution of specific feeding structures in arctic charr. This sets the stage for studies of the genetics and development of rapid and parallel craniofacial evolution.