Reproductive Transformation in the Epitokous Clam Worm, Alitta succinea (Nereididae: Annelida)

Abstract

Members of the species Alitta succinea (Phylum Annelida: Family Nereididae) are errant segmented worms with a cosmopolitan distribution around the greater Atlantic basin. Resilient mobile omnivores, these capable charismatic crawlers survive through wide ranges of temperature, salinity, dissolved oxygen, and pollutant levels. They usually live in biologically rich environments, and, as omnivores, they play an important role in stabilizing trophic levels by connecting producers to grazing mid-water predators. A. succinea reproduces via a strategy called epitoky, where upon sexually mature individuals metamorphose from a ‘crawling form’, called an atoke, into a ‘swimming form’, called an epitoke, prior to entering the water column to spawn. This dissertation takes a multidisciplinary approach to describing the reproductive biology of a population of A. succinea found in Galveston, Texas. First, we sought to understand the population dynamics of A. succinea over a two-year period to better understand their reproductive cycle. We employed traditional sampling methods and found that in Galveston Bay, numbers of A. succinea peak in the warm Summer and Fall months apparent through a substantial spike in number of small individuals. Corroborating this finding, we collected a high number of epitokes during these months indicating a primary spawning season. Although we found the greatest number of epitokes in the Summer and Fall, epitokes were collected year-round, indicating a continuous reproductive effort. All individuals collected were measured for an additional morphometric analysis. Atokes, females, and males all have unique size profiles indicative of ontogeny, where females are the largest size class. To better conceptualize the morphological differences between atokes, females and males, we analyzed their gene expression using Poly(A)- ClickSeq, an emerging economical technique for measuring relative abundance in expressed genes. We found significant differences in gene expression between the groups regarding sexualization, musculature, and visual systems. Females had a more unique genetic profile compared to atokes and males, indicating a larger regulatory network involved in feminization. CHD7, a gene associated with onset of puberty in vertebrates, was upregulated in both females and males, indicating a role in sexualization. Morphologically, musculature related genes were upregulated in atokes compared to both sexes, corroborating previous reports of muscular degeneration in epitokes. We further explored this hypothesis by imaging atokes and epitokes using micro computed tomography. We found that relative to size, epitokes have less muscle mass in their oblique muscles than atokes do. This is specifically apparent in the anterior segments, likely from atrophy of crawling muscles. In their posterior segments, we found that females and males have hypertrophied oblique muscles compared to atokes, with males to a higher degree than females. The large posterior muscles in epitokes indicate a major role in propelling the worm forward, potentially with more active parapodial movement than previously believed. Future work connecting the herein described genetic and morphological features with physiological, behavioral, and functional studies may lead to exciting discoveries in the evolution of open water annelids. Collectively, this study highlights the unique biological processes at work connecting ecology, morphology, and genetics in a comprehensive story of A. succinea reproduction.