A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes.

BACKGROUND: How novel phenotypes originate from conserved genes, processes, and tissues remains a major question in biology. Research that sets out to answer this question often focuses on the conserved genes and processes involved, an approach that explicitly excludes the impact of genetic elements that may be classified as clade-specific, even though many of these genes are known to be important for many novel, or clade-restricted, phenotypes. This is especially true for understudied phyla such as mollusks, where limited genomic and functional biology resources for members of this phylum have long hindered assessments of genetic homology and function. To address this gap, we constructed a chromosome-level genome for the gastropod Berghia stephanieae (Valdés, 2005) to investigate the expression of clade-specific genes across both novel and conserved tissue types in this species. RESULTS: The final assembled and filtered Berghia genome is comparable to other high-quality mollusk genomes in terms of size (1.05 Gb) and number of predicted genes (24,960 genes) and is highly contiguous. The proportion of upregulated, clade-specific genes varied across tissues, but with no clear trend between the proportion of clade-specific genes and the novelty of the tissue. However, more complex tissue like the brain had the highest total number of upregulated, clade-specific genes, though the ratio of upregulated clade-specific genes to the total number of upregulated genes was low. CONCLUSIONS: Our results, when combined with previous research on the impact of novel genes on phenotypic evolution, highlight the fact that the complexity of the novel tissue or behavior, the type of novelty, and the developmental timing of evolutionary modifications will all influence how novel and conserved genes interact to generate diversity.

A chromosome-level genome for the nudibranch gastropod Berghia stephanieae helps parse clade-specific gene expression in novel and conserved phenotypes.

How novel phenotypes originate from conserved genes, processes, and tissues remains a major question in biology. Research that sets out to answer this question often focuses on the conserved genes and processes involved, an approach that explicitly excludes the impact of genetic elements that may be classified as clade-specific, even though many of these genes are known to be important for many novel, or clade-restricted, phenotypes. This is especially true for understudied phyla such as mollusks, where limited genomic and functional biology resources for members of this phylum has long hindered assessments of genetic homology and function. To address this gap, we constructed a chromosome-level genome for the gastropod Berghia stephanieae (Valdés, 2005) to investigate the expression of clade-specific genes across both novel and conserved tissue types in this species. The final assembled and filtered Berghia genome is comparable to other high quality mollusk genomes in terms of size (1.05 Gb) and number of predicted genes (24,960 genes), and is highly contiguous. The proportion of upregulated, clade-specific genes varied across tissues, but with no clear trend between the proportion of clade-specific genes and the novelty of the tissue. However, more complex tissue like the brain had the highest total number of upregulated, clade-specific genes, though the ratio of upregulated clade-specific genes to the total number of upregulated genes was low. Our results, when combined with previous research on the impact of novel genes on phenotypic evolution, highlight the fact that the complexity of the novel tissue or behavior, the type of novelty, and the developmental timing of evolutionary modifications will all influence how novel and conserved genes interact to generate diversity.

Precocious Sperm Exchange in the Simultaneously Hermaphroditic Nudibranch, Berghia stephanieae.

Sexual systems vary greatly across molluscs. This diversity includes simultaneous hermaphroditism, with both sexes functional at the same time. Most nudibranch molluscs are thought to be simultaneous hermaphrodites, but detailed studies of reproductive development and timing remain rare as most species cannot be cultured in the lab. The aeolid nudibranch, Berghia stephanieae, is one such species that can be cultured through multiple generations on the benchtop. We studied B. stephanieae reproductive timing to establish when animals first exchange sperm and how long sperm can be stored. We isolated age- and size-matched individuals at sequential timepoints to learn how early individuals can exchange sperm. Individuals isolated at 10 weeks post initial feeding (wpf; ∼13 weeks postlaying [wpl]) can produce fertilized eggs. This is 6 weeks before animals first lay egg masses, indicating that sperm exchange occurs well before individuals are capable of laying eggs. Our results indicate that male gonads become functional for animals between 6 mm (∼6 wpf, ∼9 wpl) and 9 mm (∼12 wpf, ∼15 wpl) in length. That is much smaller (and sooner) than the size (and age) of individuals at first laying (12-19 mm; ∼16 wpf, ∼19 wpl), indicating that male and female functions do not develop simultaneously. We also tracked the number of fertilized eggs in each egg mass, which remained steady for the first 10-15 egg masses, followed by a decline to near-to-no fertilization. This dataset provides insights into the precise timing of the onset of functionality of the male and female reproductive systems in B. stephanieae. These data contribute to a broader understanding of reproductive development and the potential for understanding the evolution of diverse sexual systems in molluscs.

Traduit par Maryna Lesoway et Hereroa JohnstonLes stratégies de reproduction sont énormément variables chez les mollusques. Cette diversité inclut les hermaphrodites simultanés pouvant être mâle et femelle à la fois. La plupart des mollusques nudibranches sont considérés être des hermaphrodites simultanés, mais les études détaillées du développement reproductif restent rares, car la plupart des nudibranches ne peuvent pas être cultivés en laboratoire. Le nudibranche aeolid, Berghia stephanieae, est l'une des rares espèces pouvant être facilement cultivées sur plusieurs générations sur une paillasse de laboratoire. On a étudié le développement temporel reproductif de B. stephanieae dans le but d'établir à quel moment les individus font leurs premiers échanges de sperme et pour combien de temps ce dernier est gardé. Pour cela des individus ont été isolés en fonction de leur âge et de leurs tailles de manière séquentielle au cours de leurs développement afin de déterminer les premiers échanges de sperme.. Les individus isolés 10 semaines après avoir commencé de manger (∼13 semaines après avoir été pondu) sont capables de produire des œufs fertilisés. Cela se produisant 6 semaines avant que ces individus ne soient capables de déposer des masses d'œufs fécondés, indiquant que l'échange de sperme a eu lieu bien avant que ces individus aient la capacité de pondre des œufs. Nos résultats indiquent que la gonade mâle devient fonctionnelle quand les individus mesurent entre 6 mm et 9 mm de longueur. Par contraste, ces individus ne pondent pas d'œufs avant de mesurer 12 à 19 mm de longueur, indiquant que les fonctions mâles et femelles ne commencent pas en même temps. De plus, on a compté le nombre d'œufs fécondés par masse d'œufs, ce dernier restant inchangé pour les premières 10 à 15 masses d'œufs mais cela s'est suivi par un déclin rapide aboutissant à zéro œuf fécondé par masse d'œuf. Les résultats présentés ici fournissent des informations précises à propos du début du fonctionnement des systèmes reproductifs mâle et femelle chez B. stephanieae. Ces données contribuent à une compréhension approfondie du développement reproductif avec le potentiel d'une meilleure compréhension de l'évolution des diverses systèmes de reproductions.

Traducción por Daniel Escobar-CamachoLos sistemas sexuales varían ampliamente entre los moluscos. Esta diversidad incluye el hermafroditismo simultáneo, ambos sexos funcionales al mismo tiempo. Se cree que la mayoría de los moluscos nudibranquios son hermafroditas simultáneos, pero los estudios detallados del desarrollo reproductivo y su sincronización temporal son raros ya que la mayoría de las especies no se pueden mantener en el laboratorio. El nudibranquio eólido, Berghia stephanieae, es una especie que se puede mantener en cautiverio durante varias generaciones en condiciones de laboratorio. En este estudio, se analizó la sincronización del estado reproductivo de B. stephanieae para establecer el momento en el cual los animales intercambian esperma por primera vez y la duración de cuánto tiempo se puede almacenar el esperma. Para aprender cómo los individuos juveniles intercambian esperma, aislamos individuos de la misma edad y tamaño, en diferentes puntos de tiempo en una secuencia temporal. Se pudo observar que los individuos aislados a las 10 semanas, después de la primera alimentación (wpf; ∼13 semanas después de la puesta, wpl), pueden producir huevos fertilizados. Esto es 6 semanas antes de que los animales desoven masas de óvulos por primera vez, lo cual sugiere que el intercambio de esperma ocurre mucho antes de que los individuos sean capaces de desovar óvulos. Nuestros resultados indican que las gónadas masculinas se vuelven funcionales para animales de entre 6 mm (∼6 wpf, ∼9 wpl) y 9 mm (∼12 wpf, ∼15 wpl) de longitud. Este tamaño es más pequeño (y más temprano) que el tamaño (y la edad) de los individuos en su primera puesta de huevos (12­19 mm; ∼16 wpf, ∼19 wpl), lo que indica que la funcionalidad de machos y hembras no se desarrollan simultáneamente. También analizamos la cantidad de huevos fertilizados en cada masa de huevos, que se mantuvo constante durante las primeras 10 a 15 masas de huevos, seguido de una disminución de fertilización hasta casi ser nula. Estos datos proporcionan información sobre el momento preciso del inicio de la funcionalidad de los sistemas reproductivos masculino y femenino en B. stephanieae, y contribuyen a una comprensión más amplia del desarrollo reproductivo y la evolución de los diversos sistemas sexuales en los moluscos.