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Caratteri sessuali multipli e scelta femminile in Salaria pavo
Full text linkDarwin's idea of intersexual selection based on female choice was one of the most controversial parts of his theory of evolution, and only in 1982 was performed the first empirical study showing that male ornaments are favored by female choice. Since this pivotal study, several studies had demonstrated in many animal species that intersexual selection is one of most important process in evolution and speciation, as it drives the evolution of characters involved in signaling mate quality and/or species recognition. Moreover, genetic models and empirical studies had verified the Fisherian idea of self reinforcing coevolution of secondary sexual characters (SSCs) and female preference. However, the major problem left open by Darwin, the reasons why females prefer ornamented males and which benefits they could obtain from this choice, remain controversial. Female benefits can be included in two different categories: direct benefits, such as fecundity benefits, parental care, lower risk of sexually transmitted diseases and parasites, or indirect benefits, related to genetic benefits, enhancing survival or reproductive success of their offspring. If choice for males with the most elaborated traits is finalized to obtain benefits, male ornaments are expected to show a positive covariance with male qualities. This is not always the case and there are several reasons to expect that males that invest heavily in SSCs have less resources to invest on other qualities, as ejaculates qualities, parental care effort o immune system qualities. For instance in some species with alternative male reproductive strategies, an inverse relationship is observed between pre- and post-copulatory traits, with more ornamented territorial males investing relatively less in ejaculate quality compared to sneaker ones. Moreover, there is increasing evidence, mainly in birds and insects, that males face a phenotypic trade-off between investment in sexual traits and immune function.
In the last two decades, the picture is getting even more complicated by the fact that in many species females base their mate choice on multiple signals. Why this occurs is debated and many different hypotheses have been proposed. The use of multiple cues in mate choice may: (I) be adaptive and increase fitness by reducing mate choice errors or costs of choice; (II) have no influence on fitness but include preferences that are exploited by the signaler; or (III) be maladaptive and decrease fitness, as the signaler manipulates mating resistance of the receiver by taking advantage of preexisting sensory biases. Despite the fact that multiple ornaments are widespread in nature, a comprehensive analysis of the different components of male ornaments and their relationship with post-copulatory traits, and the tradeoffs between post-copulatory traits and immune function in relation to male ornamentation, has rarely been attempted before.
The aim of this project was to determine whether the different male traits signal different aspects of male quality and whether the different quality traits co-vary or are traded-off.
The model species chosen is a teleost fish, the peacock blenny, Salaria pavo (Risso,1810). This blenny is a medium sized species (up to 11 cm standard length) that exhibits a strong sexual dimorphism, with males attaining larger size than females, showing a pronounced head crest and having the first two rays of the anal fin transformed into a pair of anal glands. S. pavo is a demersal spawner with males that defend nests (usually cavities or bivalve empty shells) and guard eggs laid by several females. Females lay eggs on the nest wall in a single layer of roughly uniform density and, during breeding season, may spawn with several males. Alternative male mating tactics occurs in this species with small-sized males acting as sneakers and showing less developed SSCs. Recent studies have demonstrated that, in this species, a male sexually dimorphic trait, the anal glands (AG), produces a mucus enriched with antimicrobial substance and that males, while performing egg care, rub the anal region over the nest internal surface, likely facilitating the transfer of mucus to eggs.
The project was organized in three major parts: I) expression of male traits in relation to male mating success. II) expression of male SSCs and male qualities. III) intra and inter-relationships of male traits and quality. In the first part of this work field data about male mating success (number of eggs inside the nests and number of females playing courtship displays to males) were collected and these data were compared with male trait expression to get information on which of them are involved in male mating success. Both anal gland size and head crest appeared to contribute to male mating success. The influence of intersexual selection in the expression of these two traits was confirmed by female preference tests, where females preferred to court male dummies exhibiting a larger head crest or larger anal glands. The second part of this study was focused to investigate which information on male quality (in terms of health status and parental care) anal glands and head crest may convey to females. Two different experimental approaches were used in order to evaluate: I) the expression of pre- and post-copulatory sexual characters in male exposed to a immune challenge; II) the role of anal glands in protecting eggs from infections. To evaluate the relationship between the expression o male SSCs, their ejaculates traits and their health status, a group of males was injected with LPS, an Escherichia coli antigen, known to be a potent activator of the immune system, rapidly inducing an inflammatory response. The head crest was the only one trait showing a variation after the treatment, decreasing both in intensity and extension of its yellow coloration. To study the function of anal gland and their role in parental care three different aspects were taken into account: a) the relationship between anal gland size, anal gland weight and the protein content of their secretion; b) the activity of anal gland secretion in inhibiting the growth of 7 marine bacteria; c) the efficacy of anal gland secretion in protecting eggs from infections. Anal gland size was positively related to their mass, and with protein content of their secretion. In addition the secretion inhibited the growth of 5 of the bacterial strains tested and efficiently protected eggs against microbial infection in egg survival rate test. In the last part of the work the relationships between male SSC expression and parental care in field were analyzed and related to some parameter of innate immune system and ejaculates. Head crest size, but not anal glands or male body size, was positively related to sperm number. Anal gland size and the frequency of one behaviour related to parental care, the time spent to rubbing anal gland secretion on eggs, resulted positively related to two indices of immune stress, i.e. the ratio between number of granulocytes and lymphocytes and nitric oxide levels respectivel. Analyzing the male investment in parental care (in terms of anal gland expression plus parental behaviour) versus the investment in mating (in terms of head crest size, coloration and sperm number), a trade-off was observed.
The findings of this study highlight the role played by anal glands and head crest in the reproductive success for S. pavo males. Females preferences for males exhibiting a larger head crest have been shown by both experiments with dummies and field observations, where larger crested males were courted by more females. Head crest, and in particular its yellow coloured area, is influenced by male health status, as demonstrated by the immune challenge experiments with LPS. This E. coli antigen is known to provoke an increase of reactive oxygen species, inducing a remarkable oxidative stress in animals. The high flux of oxidants produced by the immune activation should be counteracted by the mobilization of antioxidant at the expense of the expression of sexual traits. The decrease observed in the crest yellow spot quality (in terms of both area and colour intensity) in LPS injected males strongly suggests that, in the peacock blenny, a mobilization of carotenoids, possibly responsible for the yellow colouration, may occurs in response to the oxidative stress induced by the immune challenge, as it has been observed in other species. Indeed, carotenoids are antioxidant and immuno-stimulatory compounds that are only acquired with food (i.e. not synthesized by the organism). Thus, individuals are expected to carefully optimize carotenoid allocation between competing functions: expression of coloured signals, immune response, and/or combat against oxidative stress. On this basis, the head crest colouration of peacock blenny males seems to represent an honest signal of individual condition, and may be used by female to assess male quality with respect to health status. The head crest total area, is positively related to a fertility trait: the sperm number. A positive covariance between traits used by females to assess male quality and the size or quality of the male’s ejaculate, is predicted by the phenotype-linked fertility hypothesis. Accordingly, male’s ornaments would honestly signal his fertilizing efficiency, and selection may act directly on females to choose mates that are able to fertilize all their eggs. However, so far the experimental evidences in support of this hypothesis are controversial , whereas a more powerful explanation is that intrinsically high quality males can afford to produce both better quality sperm and fancier ornaments.
The head crest of S. pavo appears to be a multi-component trait conveying information on different aspects of male quality. Indeed the extension and intensity of its colouration is related to health status, whilst its total area co-varies with fertility. Consequently, female preferences for larger and colorful head crest might be driven by the pursuit of both direct benefit, in terms of fecundity but also other benefit related to male good condition such as for instance the reduced risk of parasite transmission. However, if the good conditions have also a genetic component, not demonstrared in this study, then female might in addition gain indirect benefits in terms of quality transmissible to offspring.
The study on anal gland function provides evidences that peacock blenny males performing parental care can affect the fitness of their offspring releasing antimicrobial compound. Anal gland secretion (AGS) is active against five out of the seven bacteria species tested in this study. Three of them are common in temperate sea water and cause major fish diseases in both field and cultured marine species. Instead, M. luteus and B. sutlis have been found as occasional pathogens of freshwater fishes, and they are widely used as indicator of lysozyme activity. The finding of AGS antibacterial activity against these two species strongly indicates that the lysozyme-like substance previously described to be produced in blenny anal glands is released in their mucus secretion. The result of the egg survival experiment indicate that AGS contribute in protecting eggs from bacterial colonization. Indeed, males, while performing parental care, rub the anal urogenital region over the nest internal surface, transferring AGS secretion to eggs, and eggs deprived of this secretions have a lower probability of surviving. Both mate preference tests and field collected data showed that females, in choosing mates, care for this traits preferring individuals with more developed anal glands. Furthermore, since larger anal glands produce a secretion richer in protein and, likely in antimicrobials, female preference for larger glands, strongly suggest that female choice is driven by the direct benefit of egg protection from infections. Anal gland size e time spent to rubbing their secretion on eggs resulted respectively related with to the ratio between number of granulocytes and lymphocytes and nitric oxide levels, both two indices of immune stress. Since anal gland secret could be considered part of the parental care effort, this finding might indicated that males allocating more resources to favour offspring survivorship, increase their general stress level.
Anal glands and head crest are indicative of different male qualities, as expected by the multiple message hypothesis, predicting that different signals provide information on different individual qualities. According to this model, the signals might be evaluated together to assess the general quality of the mate, or alternatively, different receivers may pay attention to different signals. Indeed, females are often faced with multiple signals from males which convey a range of information that are not necessarily positively correlated. There are increasing evidences of a trade-off between male attractiveness and different male traits which can have profound effects on progeny fitness, such as fertility, parental care, or immune function, and female might evaluate them differently depending on whether they are choosing direct or genetic benefits. In S.pavo, male investment in parental care is negatively related to the development of head crest (a proxy of male health status and fecundity), highlighting the occurrence of a trade-off between male condition/fertility and parental qualities. If females in this species assess the general male qualities or pay attention to different qualities need further investigation.Il concetto di selezione sessuale basata sulla scelta femminile è sempre stato una delle parti più controverse della teoria evolutiva proposta da Darwin, tanto che solo nel 1982 è stato compiuto uno studio sperimentale che ha dimostrato per la prima volta che le femmine possono scelgliere il compagno riproduttivo sulla base degli ornamenti maschili. In seguito a questo primo lavoro, numerosi studi hanno dimostrato in moltissime specie animali che la selezione intersessuale è uno dei più importanti processi per l’evoluzione e la speciazione, in quanto porta allo sviluppo di caratteri connessi alla segnalazione della qualità del compagno riproduttivo e/o al riconoscimento dei conspecifici. Inoltre, sia modelli genetici che studi sperimentali hanno dimostrato l’idea fischeriana della coevoluzione auto rinforzante dei caratteri sessuali secondari (CSS) e della preferenza femminile. Tuttavia, il problema cruciale della teoria Darwiniana, cioè la ragione per cui le femmine debbano preferire gli individui con ornamenti più sviluppati, e quali benefici possano ottenere da questa scelta, rimane ancora controverso.
I benefici che le femmine possono ottenere possono essere raggruppati in due differenti categorie: benefici diretti, come ad esempio una maggiore fecondità, migliori cure parentali o un minor rischio di contrarre infezione durante l’accoppiamento, oppure in benefici indiretti, legati a benefici genetici che aumentano la sopravvivenza o il successo riproduttivo della prole. Se la scelta femminile è volta ad ottenere benefici, allora è lecito aspettarsi che lo sviluppo dei CSS e la qualità dei maschi siano tra loro correlati positivamente. Questo in realtà non è sempre vero, e esistono diversi motivi per cui invece i maschi che investono maggiormente nello sviluppo dei CSS possano non avere sufficienti risorse per le altre qualità, come ad esempio le cure parentali, l’investimento per la produzione di spermi e per il sistema immunitario. Ad esempio in alcuni casi, in specie in cui sono presenti tattiche riproduttive alternative, i maschi territoriali, che hanno CSS più sviluppati, producono eiaculati di minor qualità rispetto ai maschi che parassitano gli accoppiamenti. Inoltre, esiste un sempre maggior numero di testimonianze che in molte specie, soprattutto insetti e uccelli, siano presenti compromessi tra l’investimento in CSS e l’investimento per il sistema immunitario.
La comprensione dei meccanismi di selezione intersessuale risulta ancora più complicata, se si considera che nell’ultimo ventennio ci si è resi conto che in molte specie le femmine basano la scelta del compagno non su un singolo tratto, ma sulla base di caratteri multipli. Il perché di questa contemporanea presenza di più tratti è tuttora dibattuta, e ha portato alla formulazione di diverse ipotesi. L’uso dei tratti multipli potrebbe essere: I) adattativa, se aumenta la fitness della femmina riducendo il costo della scelta e la possibilità di errori; II) non avere influenza sulla fitness della femmina, ma essere dovuta al mantenimento di preferenze femminili innate o sviluppatesi in altri contesti e con altre funzioni; III) disadattativa, se diminuisce la fitness delle femmine, in quando i maschi sfruttano bias sensoriali per manipolare la scelta femminile.
Lo scopo di questo progetto è stato quello di determinare se i diversi tratti esibiti dai maschi siano informativi e, se si, di quali qualità maschili. Inoltre, ha cercato di valutare la possibile presenza di compromessi tra l’investimento maschile in alcuni tratti o qualità a discapito dell’investimento in altri. Infatti, sebbene la presenza di CSS multipli sia molto diffusa nel regno animale, raramente si sono condotti studi che abbiano cercato di valutare tutte le diverse componenti dei tratti maschili e la possibile presenza di compromessi tra l’investimento per il loro sviluppo e l’investimento in tratti post-copulatori o del sistema immunitario.
La specie modello scelta per questo lavoro è Salaria Pavo (Risso, 1810). Salaria pavo è un blennide di medie dimensioni (lunghezza massima 15 cm), che presenta un forte dimorfismo sessuale, in cui i maschi hanno dimensioni maggiori rispetto alle femmine, esibiscono una vistosa cresta cefalica e hanno i primi due raggi della pinna anale modificati in una coppia di ghiandole anali. Durante la stagione riproduttiva i maschi difendono un nido (generalmente una cavità nella roccia o un guscio vuoto di bivalve) in cui diverse femmine depongono uova di tipo demerso, incollandole in singolo strato alle pareti interne del nido. Il maschio poi difenderà le uova, compiendo cure parentali su di esse, sino alla schiusa. In questa specie è stata inoltre descritta la presenza di tattiche riproduttive alternative, con maschi piccoli e che non hanno CSS sviluppati che parassitano gli accoppiamenti dei maschi territoriali. Studi recenti hanno inoltre dimostrato che il secreto delle ghiandole anali produce un muco ricco di una sostanza con potere antimicrobico. È stato ipotizzato che i maschi spalmino questo secreto sulle uova durante le cure parentali.
Il progetto è stato organizzato in tre parti: I) studio della relazione fra l’espressione dei caratteri maschili dimorfici e il successo di accoppiamento; II) studio della relazione fra lo sviluppo dei caratteri sessuali secondari dei maschi e le loro possibili qualità; III) studio delle relazioni tra diversi aspetti dell’investimento riproduttivo. Durante la prima fase sono stati raccolti in natura i dati del successo di accoppiamento dei maschi (numero di uova nel nido e numero di display di corteggiamento femminili ricevuti) e confrontati con lo sviluppo dei tratti maschili. Sia la ghiandole anali che la cresta cefalica sono risultati tratti che hanno influenza sul successo di accoppiamento maschile. Con esperimenti di preferenza femminile si è inoltre dimostrato che questi tratti sono sottoposti a selezione intersessuale, in quanto le femmine hanno preferito corteggiare di maschi che avevano creste e ghiandole maggiormente sviluppate. La seconda parte del lavoro è stata incentrata sulla valutazione delle informazioni sulla qualità dei maschi che le femmine possono ricavare valutando i maschi sulla base di questi due CSS. Questo studio è stato affrontato con due differenti approcci, per valutare: a) l’espressione dei caratteri sia pre che postcopulatori in maschi sottoposti ad uno stress immunitario; b) il ruolo svolto dalle ghiandole anali nella protezione delle uova da infezioni. Per valutare il legame tra l’espressione dei CSS maschili, la qualità del loro eiaculato e lo stato di salute, un gruppo di maschi è stato trattato con iniezione di LPS, un antigene di Escherichia coli, che è un potente attivatore del sistema immunitario che induce rapidamente una risposta infiammatoria. La cresta è risultata l’unico tratto a subire l’influenza del trattamento, mostrando una diminuzione sia nell’estensione che nell’intensità della sua colorazione gialla. Per valutare il ruolo delle ghiandole anali nella protezione delle uova sono state studiate tre diverse caratteristiche: a) la relazione tra le dimensioni delle ghiandole e il contenuto proteico del loro secreto; b) l’attività antimicrobica del loro secreto contro 7 diversi ceppi batterici marini; c) l’efficacia del secreto nell’aumentare la sopravvivenza delle uova. Le dimensioni delle ghiandole anali sono risultate positivamente correlate con il contenuto proteico della loro secrezione, secrezione che è risultata inoltre avere potere antimicrobico, inibendo la crescita di 5 dei 7 ceppi batterici testati e proteggendo le uova da infezioni batteriche. Nella terza e ultima parte del lavoro sono stati raccolti dati sul campo relativi all’apporto delle cure parentali sulle uova di un gruppo di maschi. Questi dati sono quindi stati confrontati con le caratteristiche maschili, sia in termini dello sviluppo dei CSS, che in qualità dell’eiaculato e stato del sistema immunitario. L’investimento complessivo in cure parentali (considerando sia le ghiandole anali che alcuni comportamenti) è risultato negativamente correlato con l’investimento per l’ac
When fathers make the difference: efficacy of male sexually selected antimicrobial glands in enhancing fish hatching success
No full text1. Egg and offspring resistance to pathogens is a major determinant of survival and has been
mainly ascribed to maternal factors. However, paternal production of antimicrobials was
recently suggested to increase offspring survival in species where males perform egg care.
2. In the peacock blenny, Salaria pavo, a demersal spawning species where males exhibit a pair of
anal glands producing lysozyme-like compounds, we tested the antimicrobial activity and the
egg protection efficacy of these glands. The anal gland secretion (AGS) has an inhibitory effect
on the growth of both Gram-negative and Gram-positive bacteria, including those causing the
most severe fish diseases in marine culture. The egg clutches cared for by males deprived of anal
glands have a significantly lower survival rate than those cared for by sham-operated males and
non-viable eggs showed clear signs of bacterial infection.
3. Anal gland secretion production and its protein content are proportional to gland size. In species
where male parental care plays a crucial role in offspring survival, females are expected to
assess mates selecting those traits that are reliably associated with parental ability. Hence, we
experimentally challenged females with dummy males differing in anal gland size. Females definitely
preferred dummy males with larger anal glands, suggesting that their choice is driven by
the pursuit of direct fecundity benefits.
4. These findings indicate that antimicrobial production is a crucial component of male parental
care. The contribution of antimicrobials to male performance as fathers suggests that the development
of traits devoted to this function may influence male attractiveness and be sexually
selected
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No full textWe have done our best to complete the author checklist relating to the use of animals in the hut study. Note that the objective for the hut study was to evaluate the IRS treatment applications for residual efficacy against Anopheles mosquitoes, including the local An. coluzzii mosquito population. Cows were only used to attract mosquitoes into the huts and no tests were carried out directly on the cows. The author checklist is intended for use with studies where experiments are carried out on animals, which is why we have had such difficulty in completing this for the hut study, as many of the questions do not relate to how the cows were used
Author-wise bibliometric analysis based on entropy.
No full textAuthor-wise bibliometric analysis based on entropy.</p
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