A Male Poecillid's Sexually Dimorphic Body Plan, Behavior, and Nervous System

Abstract

Here we review the literature of a male poecillid's sexually dimorphic body plan, behavior, and nervous system, including work dating from the mid 1800s to the mid 1990s as well as work in press or in preparation for publication. Rosa-Molinar described the remodeling of the sexually dimorphic anal fin appendicular support, confirmed earlier claims about the development of the male and female secondary sex characteristics in the Western Mosquitofish, Gambusia affinis and provided for the first time direct embryonic evidence suggesting that remodeling of the sexually dimorphic anal fin appendicular support is biphasic. The first process begins in embryos and proceeds similarly in immature males and females; the second process occurs only in males and results in the anterior transposition of the anal fin and its appendicular support to the level of vertebra 11 [Rosa-Molinar E, Hendricks SE, Rodriguez-Sierra JF, Fritzsch B. 1994. Development of the anal fin appendicular support in the western mosquitofish, Gambusia affinis (Baird and Girard, 1854): a reinvestigation and reinterpretation. Acta Anat 151:20-35.] and the formation of a gonopodium used for internal fertilization. Studies using high-speed video cameras confirmed and extended Peden's and others' observations of copulatory behavior. The cameras showed that circumduction is a complex movement combining in a very fast sequence abduction, extension and pronation, S-start-type fast-start (defined as torque-thrust), and adduction movements. Recent work on the nervous system demonstrated dye-coupling between motor neurons and interneurons via gap junctions, suggesting an attractive substrate for the rapid motions involved in poecillid copulatory reflexes.

Origins of female genital diversity: Predation risk and lock-and-key explain rapid divergence during an adaptive radiation

“…First, copulatory behaviors of Gambusia fishes represent some of the most sophisticated and rapid behaviors known in fishes (Rivera‐Rivera et al. ). For successful copulation, a male must accurately place the tip of the gonopodium into a very small genital opening while performing a complicated torque‐thrust maneuver that takes only 20–50 ms.…”

Fine-scale genital morphology affects male ejaculation success: an experimental test

“…Poeciliid fishes exhibit internal fertilization involving one of the briefest copulations known (20-50 ms; electronic supplementary material, Video S1). Males employ a coercive torque-thrust motion [11], whereby a male twists his body, swings his gonopodium (a modified anal fin) forward and expels spermatophores into the female's genital tract along a groove formed by the folded gonopodium [12][13][14]. Females are usually unreceptive, so there is strong selection on males to mate coercively [15].…”

Abundance of gap junctions at glutamatergic mixed synapses in adult Mosquitofish spinal cord neurons

“…Gap junctions at these glutamatergic mixed synapses are extraordinarily abundant in the 14th spinal segment (Figures 6–7 ), the main spinal segment that innervates the male sexually dimorphic genitalia, the gonopodium (Rosa-Molinar, 2005 ; Rivera-Rivera et al, 2010 ). Gap junctions are much less abundant in the 16th spinal segment and in the more rostral (1–7) spinal segments and in the more caudal (17–33) spinal segments of the adult (male and female) Mosquitofish spinal cord (data not shown).…”

“…To assist in understanding gap junctions’ role in fast motor behavior, we used a minimally-invasive neural-tract-tracing/labeling technique to introduce either gap junction-permeant or -impermeant dyes into deep muscles controlling the gonopodium (a sexually dimorphic sperm transferring organ) of a “reference species”, the adult male Western Mosquitofish, Gambusia affinis (Mosquitofish) a small, sexually dimorphic teleost fish whose radical remodeling and shifting of the axial and appendicular musculoskeletal support facilitates an extremely rapid movement of the gonopodium to transfer encapsulated sperm bundles, spermatozeugmata, into the adult female reproductive tract (Rosa-Molinar et al, 1994 , 1996 , 1998 ; Rosa-Molinar, 2005 ; Rivera-Rivera et al, 2010 ).…”

“…To transfer spermatozeugmata, the male Mosquitofish body bends into an “S-shaped fast-start” curvature defined as “torque” (Figure 1 ); simultaneously the gonopodium makes an extremely rapid directional movement defined as “thrust” (Figure 1 ; Weihs, 1973 ; Webb, 1976 ; Harper and Blake, 1990 , 1991 ; Johnston et al, 1995 ; Rosa-Molinar et al, 1996 ; Domenici and Blake, 1997 ; Spierts and Leeuwen, 1999 ; Hale, 2002 ; Rosa-Molinar, 2005 ; Rivera-Rivera et al, 2010 ). The speed of the “torque/thrust” maneuver (complete in <20 mS), particularly of the “thrust” component, suggests that electrical and not chemical synapses are involved in controlling the finer aspects of Mosquitofish rapid motor behavior.…”