Alexa Bely - Univ. of Maryland

Animals vary dramatically in their ability to replace lost body parts through regeneration. To elucidate the developmental mechanisms by which regeneration abilities evolve, we are studying closely related species of naidine annelids (a group of small, asexually-reproducing aquatic oligochaetes) that differ markedly in their regeneration abilities. While many naidines have extensive abilities to regenerate parts of their anterior/posterior body axis, we have identified several species that have recently and independently lost the capacity for anterior regeneration. Which developmental processes fail in non-regenerating species? Do the same developmental processes fail in different lineages that have independently lost regeneration abilities? We are investigating cellular and molecular processes in closely related regenerating and non-regenerating species pairs to address questions such as these. Current and future studies include characterizing wound healing, blastema formation, cell migration, body-patterning, and stem cell distribution. Parallel investigations of several lineages that have independently lost regeneration abilities provide the opportunity to identify developmental processes that may be particularly prone to being blocked during evolution

click on photos for larger, labeled images


a naidine oligochaete, Pristina leidyi, regenerating a new head	another naidine, Paranais litoralis, that has lost the ability to regenerate a new head

At least two naidine lineages (orange) have independently lost the ability to regenerate a head. Ability to regenerate a new head is mapped onto a tree of naidine genera based on the mitochondrial gene COI.
Black: genera containing species that can regenerate a new head
Orange: genera containing species that can not regenerate a new head

Modification of the anterior-posterior axis during agametic reproduction
The anterior-posterior axis is a defining feature of the Bilateria. In the vast majority of bilaterians the A/P axis always exists singly; the animal possesses just one anterior end and one posterior end. Remarkably, a few bilaterian groups have evolved the ability to reproduce agametically (e.g., by fission, budding), during which the A/P axis may be dramatically altered. These organisms challenge our notion of a single fixed A/P axis and clearly demonstrate that the A/P axis can be malleable during the course of the life cycle, as well as during the course of evolution. The A/P axis can become subdivided into multiple tandemly arrayed axes (e.g., in annelids and platyhelminths undergoing paratomic fission, "B" below), it can become branched (e.g., in colonial hemichordates and annelids undergoing stolonization, "C" below), and it can even give rise to axes with opposite orientations (e.g., in acoels undergoing reversed-polarity budding, "D" below). How, at the developmental level, does a single body axis become modified into multiple axes? We are investigating this question in naidine annelids reproducing by paratomic fission and in an acoel reproducing by reversed polarity budding, focusing primarily on expression of body axis patterning genes such as Hox genes.

Paratomic fission in naidine annelids
Paratomic fission is an unusual mode of reproduction that has evolved multiple times among bilaterian animals, including several times among annelids. During paratomic fission, a new anterior end and a new posterior end are intercalated in the middle of the body, forming transiently linked chains of individuals which remain physiologically and behaviorally coordinated until they ultimately separate. By this process, then, the original body axis of the worm is essentially “broken” into two (or more) consecutive axes, long before the worm physically separates into multiple worms. The largest group of fissioning annelids, including over one hundred described species, are the naidines, which are tiny, delicate aquatic oligochaetes commonly found in lakes, ponds, and streams.

Reproduction by paratomic fission in naidines, by which one A/P axis becomes divided into two or more tandemly arrayed axes.

Paratomic fission, in which a new head and tail are intercalated in the middle of the parental worm's body. Fission is initiated when a midbody segment develops a zone of cell proliferation (dark bar in middle of body). This zone, called a fission zone, splits into two proliferating zones, each forming new tissue anteriorly. The anterior zone forms a new tail (blue) for the anterior part of the worm, and the posterior zone forms a new head (green) for the posterior part of the worm.

a naidine oligochaete, Paranais litoralis,
reproducing by paratomic fission
[click on photo for larger, labeled image]

Reversed-polarity budding and fission in acoels of the genus Convolutriloba
Reversed-polarity budding is a remarkable process known from only a single bilaterian species: the acoel Convolutriloba retrogemma. This species produces offspring at the posterior end of the original worm, with buds oriented in the opposite direction from the parent. A two-headed, and often three-headed (since two posterior buds can be produced at once), worm is thus produced. Late-stage buds appear to move independently of the parent and eventually tear away from it. The two other known species in the genus Convolutriloba, C. hastifera and C. longifissura, also reproduce asexually. C. hastifera reproduces by a simple transverse fission and C. longifissura reproduces by two orthogonal fissions, the first transverse and the second longitudinal (a highly unusual plane of fission in bilaterians). Convolutriloba species are tropical and marine and frequently find their way into marine aquaria, where they can be considered pests.

Reproduction by reversed-polarity budding in the acoel Convolutriloba retrogemma, during which buds are produced with an A/P axis rotated 180 degrees relative to that of the parent.