American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Miniaturization, genome size, and biological size in a diverse clade of salamanders”

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Louis Paul Decena-Segarra, Lilijana Bizjak-Mali, Aleš Kladnik, Stanley K. Sessions, and Sean M. Rovito (Nov 2020)

Miniature salamanders have reduced genome sizes compared to larger species

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Tiny salamanders are “bigger” than we thought

<i>Thorius macdougalli</i>, one of the world’s smallest salamanders, on a Mexican 10-peso coin.<br />(Credit: Louis Paul Decena-Segarra)
Thorius macdougalli, one of the world’s smallest salamanders, on a Mexican 10-peso coin.
(Credit: Louis Paul Decena-Segarra)

The smallest salamanders in the world are found in Mexico; they are under 3.5 cm (about 1.5 in) long and have heads smaller than a pencil eraser. Not only do they have to fit their eyes, brains, and other organs into a very small space, but they also face challenges posed by large genome size (the total amount of DNA per cell). All salamanders have very big genomes (four to almost 40 times as big as the human genome), meaning these salamanders have to make all of their sensory organs (made up of big cells) fit into the small space available in their heads. As part of a collaboration between scientists at the Advanced Genomics Unit in Mexico, the University of Ljubljana, Slovenia, and Hartwick College, USA, Paul Decena (a masters student from Mexico) and his collaborators measured the genome size of Mexican salamanders and tested the prediction that smaller salamanders would have smaller genomes to avoid problems associated with making tiny organs out of big cells. They also quantify “biological size”, which measures how big the physical size of organisms is relative to their genome (and cell) size. They find support for a relationship between genome size and cell size and report the smallest salamander genome recorded to date (about three times as big as the human genome). They also show that some tiny salamanders are biologically “bigger” than others and that some salamanders that are not physically miniature have such large genomes that they are biologically “smaller” than miniature species. These results help us understand how body size impacts genome size (or perhaps the reverse) and open the door to sequencing complete salamander genomes by finding some small enough to be sequenced using available methods.

<i>Bolitoglossa franklini</i>, one of the salamanders with the largest genome size measured to date.<br />(Credit: Sean M. Rovito)
Bolitoglossa franklini, one of the salamanders with the largest genome size measured to date.
(Credit: Sean M. Rovito)

Algunas salamandras miniatura son más “grandes” de lo que pensábamos

Las salamandras más pequeñas del mundo se encuentran en México, miden menos de 3.5 cm (1.5 in) de longitud y sus cabezas son más pequeñas que un borrador de un lápiz. Además de tener que acomodar sus ojos, cerebro y órganos en espacios muy pequeños, también tienen que lidiar con retos impuestos por sus grandes tamaños del genoma (la cantidad de ADN por célula). Todas las salamandras tienen genomas gigantes (cuatro a 40 veces más grandes que el genoma humano), por lo que estás salamandras tienen que hacer que sus órganos sensoriales (formados por células grandes) quepan en el espacio disponible en sus cabezas. Como parte de una colaboración entre científicos de la Unidad de Genómica Avanzada en México, La Universidad de Ljubljana, Slovenia, y el Hatwick College, USA, Paul Decena (estudiante de maestría en México) y sus colaboradores midieron el tamaño del genoma de salamandras Mexicanas, y probaron la predicción de que las salamandras más pequeñas tienen genomas reducidos para evitar algunos de los problemas asociados con hacer organos pequeños con células grandes. También cuantificaron el “tamaño biológico”, que mide qué tan grande es un organismo en relación al tamaño del genoma y de sus células. También encontraron soporte para una relación entre el tamaño del genoma y el tamaño de la célula, y reportan el tamaño del genoma más pequeño encontrado en una salamandra hasta la fecha (casi tres veces más grande que el genoma humano). También encontraron que algunas salamandras son biológicamente “más grandes” que otras y que algunas salamandras que no son miniatura por sus medidas físicas tienen genomas tan grandes que en realidad son “más pequeñas” que las salamandras miniatura. Estos resultados pueden ayudarnos a entender como el tamaño del cuerpo impacta en el tamaño del genoma (o visceversa) y abre la puerta para secuenciar los genomas completos de algunas salamandras con genomas relativamente pequeños con los métodos disponibles actualmente.


An adult and juvenile of <i>Isthmura bellii</i>, one of the world’s largest lungless salamanders.<br />(Credit: Sean M. Rovito)
An adult and juvenile of Isthmura bellii, one of the world’s largest lungless salamanders.
(Credit: Sean M. Rovito)

Abstract

Genome size (C-value) can affect organismal traits across levels of biological organization, from tissue complexity to metabolism. Neotropical salamanders show wide variation in genome and body sizes, including several clades with miniature species. Because miniaturization imposes strong constraints on morphology and development, and genome size is strongly correlated with cell size, we hypothesize that body size has played an important role in the evolution of genome size in bolitoglossine salamanders. If this hypothesis is correct, then genome size and body size should be correlated in this group. Using Feulgen Image Analysis Densitometry (FIAD), we estimated genome sizes for 60 species of neotropical salamanders. We also estimated the “biological size” of species by comparing genome size and physical body sizes in a phylogenetic context. We found a significant correlation between C-value and physical body size using optimal regression with an Ornstein-Uhlenbeck model, and report the smallest salamander genome found to date. Our index of biological size showed that some salamanders with large physical body size have smaller biological body size than some miniature species, and that several clades showed patterns of increased or decreased biological size compared to their physical size. Our results suggest a causal relationship between physical body size and genome size and show the importance of considering the impact of both on the biological size of organisms. Indeed, biological size may be a more appropriate measure than physical size when considering phenotypic consequences of genome size evolution in many groups.