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Summa the Plainfin Midshipman Porichthys Nota

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ALTERNATIVE LIFE HISTORY STRATEGIES AND DIMORPHIC MALES IN AN ACOUSTIC COMMUNICATION SYSTEM Andrew H. Bass Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853. ~Summa collected by seining in offshore feeding sites!. Studiesof nesting males and femalesrevealed that The plainfin midshipman Porichthys parentalmate-calling males,which we designatedas notatus! has two male reproductive morphs: Nest- "Type I", had an eight-fold larger body massthan a building "Type I" males generatelong duration, quasi- secondgroup of "Type II" males. By contrast, Type sinusoidal-like, advertisement calls "hums"! to attract II males had on averagea nine-fold larger GSI. femalesto nestsand trains of short duration agonistic Lastly, there were dramatic dimorphisms in vocal calls "grunts"! in defenseof their egg clutch and nest musculature. The vocal musclesof midshipman are a againstpotential intruder males.Sneak/satellite- pair of skeletalmuscles attached to the lateral walls of spawning "Type II" males do ~nt build nests,guard their swimbladder; their contraction rate establishes a eggsor acoustically court females; like females,they vocalization's fundamental frequency, which is under infrequently generateisolated grunts in non-spawning the control of a brainstemmotor pathway Bass and contexts. Studies of vocal motor traits indicate Baker 1990, 1991!. The mass of the Type I male distinct, non-overlappingdevelopmental trajectories vocal musculaturewas severalfold larger than that of for Type I and II males, while otolith analysesshow Type II males or females!, consistentwith the robust that Type II males are sexually precociouscompared ability of Type I males to produce hums continuously to Type I males. Thus, compared to Type II males, for long periods of time, often on the order of Type Is have an extendedjuvenile stageduring which minutes. The relatively small vocal muscle in Type II they are investing in body growth and a vocal motor malesand femalesis paralleled by their apparent system. In contrast, Type II males are investing in ability to infrequently generateisolated, low amplitude earlier reproduction. grunts Bass and Baker, 1990; Brantley and Bass, 1994!. Sexual polymorphisms in the vocal muscle Alternative Male Re roductive Mo hs Overview were paralleledby dimorphisms in the sizesof motoneurons that innervate the muscles Bass and Since the turn of the century, Marchaterre, 1989b!. midshipman Porichthys notatus! have been known to The early studies also showed generatean unusualsinusoidal-like vocalization dimorphisms in the most fundamentalcharacters of "hum"! during the breeding season review: Bass, skeletal muscle Z-lines, sarcoplasmicreticulum, 1990!. Studiesof captive populations of midshipman mitochondria density!, motor axons cross sectional show that hums apparentlyfunction as acoustic area,the size of neuromuscularjunctions, and courtship displays usedby parentalmales to attract synaptic vesicle density! and the morphology of gravid females to their nests Brantley and Bass, physiologically-identified vocal motor neuronsand 1994!. This hypothesis was confirmed in playbacks their presynaptic,pacemaker neurons review: Bass, of computer-synthesizedhums through underwater 1992!. Intracellular staining and recording studies speakers McKibben et al., 1995; also seeIbara et demonstrateddimorphisms in the soma-dendritic al., 1983!. Parentalmales also generatelong trains of dimensionsand the oscillatory-like firing frequency of 50-150 msecduration "grunts" when challengedby individual motoneuronsand pacemakerneurons. All intruder males Type I or II; seeBrantley and Bass, vocal traits are greaterin magnitudeamong the mate- 1994!. Playbacksof grunts are not attractive to gravid calling Type I males; this includes the firing frequency females McKibben et al., 1995!. of the central motor pathway which is 20% higher and Early in our studies,we discovered matchesthe higher fundamentalfrequency of their alternativemale reproductivephenotypes in vocalizations Bass and Baker, 1990; Brantley and midshipmanon the basis of a suiteof somatic traits- Bass, 1994!. body size, gonadosomaticindex GSI, ratio of gonad Neuroendocrinestudies of midshipman weight to body weight!, and the size of vocal muscles have focusedon two traits: gonadal steroids and and vocal motoneurons Bass and Marchaterre, GnRH-like immunoreactive ir! neurons. There are 1989a,b; also seeBrantley et al., 1993a!. Only morph-typical circulating levels of gonadal steroids reproductively active adults Type I and II males and Brantley et al., 1993b!. Type I and II males and females are found in nest sites juveniles are only femalesexhibited contrastingsteroid hormone 25$ profiles. 11-ketotestosteronewas the predominant traits Marchaterreet al., in press!. The biocytin androgenin Type I males; testosteronealone was method identified significant Student t-test; p<0.05! detectablein Type II males and females,while 178- increases in the cross-sectional area of motor 0%!, estradiol was detectableonly among females. A pacemaker0%!, and ventral medullary 5%! separateimmunocytochemical study identified age-, neuronsamong androgen-treatedjuvenile males n=9! sex- and male morph-specific patternsin the size and comparedto controls matchedfor body size n=10; number of GnRH-ir neuronsin the preoptic area p>0.7!. Androgen treatmentsincluded the non- POA! Grober et al., 1994!. The data suggestedthat aromatizableandrogens 11-ketotestosterone and the POA-pituitary/ GnRH-gonadotropinaxis initiates dihydrotestosterone,and testosteronepropionate; their sexualmaturation events at different agesin Types I effects did not differ p>0.2!. and II males also see Bass, 1993!. Otolith studies Neurophysiological studies next have confirmed this and show that Type II males identified increases in two traits: fundamental matureabout I year earlier thanType I males A. dischargefrequency FDF! and "fatigue resistance" Bass and E. Brothers, unpub. observ.!. FR! among androgen-treatedjuveniles. FDF refers to the highly stable standarddeviation of 1.1-1.2 Hz! Onto en of Andro en-Sensitive Vocal Traits firing frequency of the central motor circuit Bass and Baker, 1990!. As noted earlier, a Type I male's vocal Among juvenile midshipman,there is a phenotypeis characterizedby vocalizationsand a divergencein muscle phenotypeat about 1 yearof age motor volley with a FDF 20% higher than females, Brantley et al., 1993a!: Only juvenile Type I males Type II males, or juveniles. Androgens induced a experiencea pre-maturational,4-fold increasein fiber significant p<0.05! 13% increasein FDF in number followed at sexual maturity by a sudden androgen-treatedjuveniles n=4!! comparedto increasein fiber size. Relative to body mass,this untreatedcontrols n=7; there was no significant resultsin a 6-fold greatervocal muscle massin adult difference in body size betweenthe test groups, Type I males. Androgen, and not estrogenor p>0.3!. The ability of Type I males to generatelong cholesterol,treatments of juvenile males and females duration mate calls is paralleledby the ability to evoke markedly increasedsonic muscle size which included a rhythmic motor volley for long time periods using changesin muscle fiber number and structure central brain stimulation - the systemseemingly does Brantley et al., 1993c!. not fatigue. The following experiment was carried out Biocytin, a low molecular weight complex to quantify the vocal system'sFR: A train of low of biotin and lysine, is transportedtransneuronally in amplitude, midbrain stimuli were delivered 10 times at the vocal system of midshipman. Thus, a single 1 ms intervals during a trial see Bass and Baker, application of biocytin to the cut end of a sonicnerve 1990for methods!. Ten trials, each separatedby a 10 at the level of the swimbladder results in a labe!ling, minute rest period, constituted a single experiment. we propose, of all neuronsin the brain forming a FR was defined as the percentageof stimulus trains vocal motor network Bass et al., 1994!. This over the entire experimentthat evoked a rhythmic includesa pacemaker-motoneuroncircuit and a ventral volley. As predictedby the vocal behaviorof each medullary nucleusthat links the pacemakercircuitry reproductive morph, FR is 1-3 fold higher in Type I bilaterally. Importantly, surgical isolation of the malescompared to females and Type II males. There brainstemregion inclusive of motor, pacemakerand is also a significant p<0.05! 47% increasein FR ventral medullary neuronsappears both necessaryand among androgen-treatedjuveniles comparedto sufficient for generatinga rhythmic vocal motor controls. FR and FDF were unchangedin two 178- discharge. We have now exploited the biocytin estradiol-treatedjuveniles p>0.3!. methodfor mapping to study the ontogenyof the Together, the data suggeststhat proposedvocal motor circuit. The results show that androgen-sensitiveevents can account for the increasesin motoneuronsoma size among nascent! developmentof the Type I male vocal motor juvenile Type I males parallel the developmentof phenotype. dimorphisms in vocal muscle fiber number. There were also parallel increasesin the size of pacemaker Concludin Comments and ventral medullary neurons,although more modest in magnitude.Thus, sexual maturation of the Type I Growth patterns, age and size at sexual male's mate calling circuit parallels the ontogenyof its maturity are examplesof life history traits Stearns, target muscle Horvath et al., 1994!. 1992!. The data presentedhere suggeststhat Androgen pellet implants have also been
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