Segmentation of the millipede trunk as suggested by a homeotic mutant with six extra pairs of gonopods

TY - JOUR

T1 - Segmentation of the millipede trunk as suggested by a homeotic mutant with six extra pairs of gonopods

AU - Akkari, Nesrine

AU - Enghoff, Henrik

AU - Minelli, Alessandro

PY - 2014/1/17

Y1 - 2014/1/17

N2 - Background: The mismatch between dorsal and ventral trunk features along the millipede trunk was long a subject of controversy, largely resting on alternative interpretations of segmentation. Most models of arthropod segmentation presuppose a strict sequential antero-posterior specification of trunk segments, whereas alternative models involve the early delineation of a limited number of 'primary segments' followed by their sequential stereotypic subdivision into 2n definitive segments. The 'primary segments' should be intended as units identified by molecular markers, rather than as overt morphological entities. Two predictions were suggested to test the plausibility of multiple-duplication models of segmentation: first, a specific pattern of evolvability of segment number in those arthropod clades in which segment number is not fixed (e.g., epimorphic centipedes and millipedes); second, the occurrence of discrete multisegmental patterns due to early, initially contiguous positional markers.Results: We describe a unique case of a homeotic millipede with 6 extra pairs of ectopic gonopods replacing walking legs on rings 8 (leg-pairs 10-11), 15 (leg-pairs 24-25) and 16 (leg-pairs 26-27); we discuss the segmental distribution of these appendages in the framework of alternative models of segmentation and present an interpretation of the origin of the distribution of the additional gonopods.The anterior set of contiguous gonopods (those normally occurring on ring 7 plus the first set of ectopic ones on ring 8) is reiterated by the posterior set (on rings 15-16) after exactly 16 leg positions along the AP body axis. This suggests that a body section including 16 leg pairs could be a module deriving from 4 cycles of regular binary splitting of an embryonic 'primary segment'.Conclusions: A very likely early determination of the sites of the future metamorphosis of walking legs into gonopods and a segmentation process according to the multiplicative model may provide a detailed explanation for the distribution of the extra gonopods in the homeotic specimen. The hypothesized steps of segmentation are similar in both a normal and the studied homeotic specimen. The difference between them would consist in the size of the embryonic trunk region endowed with a positional marker whose presence will later determine the replacement of walking legs by gonopods.

AB - Background: The mismatch between dorsal and ventral trunk features along the millipede trunk was long a subject of controversy, largely resting on alternative interpretations of segmentation. Most models of arthropod segmentation presuppose a strict sequential antero-posterior specification of trunk segments, whereas alternative models involve the early delineation of a limited number of 'primary segments' followed by their sequential stereotypic subdivision into 2n definitive segments. The 'primary segments' should be intended as units identified by molecular markers, rather than as overt morphological entities. Two predictions were suggested to test the plausibility of multiple-duplication models of segmentation: first, a specific pattern of evolvability of segment number in those arthropod clades in which segment number is not fixed (e.g., epimorphic centipedes and millipedes); second, the occurrence of discrete multisegmental patterns due to early, initially contiguous positional markers.Results: We describe a unique case of a homeotic millipede with 6 extra pairs of ectopic gonopods replacing walking legs on rings 8 (leg-pairs 10-11), 15 (leg-pairs 24-25) and 16 (leg-pairs 26-27); we discuss the segmental distribution of these appendages in the framework of alternative models of segmentation and present an interpretation of the origin of the distribution of the additional gonopods.The anterior set of contiguous gonopods (those normally occurring on ring 7 plus the first set of ectopic ones on ring 8) is reiterated by the posterior set (on rings 15-16) after exactly 16 leg positions along the AP body axis. This suggests that a body section including 16 leg pairs could be a module deriving from 4 cycles of regular binary splitting of an embryonic 'primary segment'.Conclusions: A very likely early determination of the sites of the future metamorphosis of walking legs into gonopods and a segmentation process according to the multiplicative model may provide a detailed explanation for the distribution of the extra gonopods in the homeotic specimen. The hypothesized steps of segmentation are similar in both a normal and the studied homeotic specimen. The difference between them would consist in the size of the embryonic trunk region endowed with a positional marker whose presence will later determine the replacement of walking legs by gonopods.

U2 - 10.1186/1742-9994-11-6

DO - 10.1186/1742-9994-11-6

M3 - Journal article

C2 - 24438178

SN - 1742-9994

VL - 11

JO - Frontiers in Zoology

JF - Frontiers in Zoology

M1 - 6

ER -