Evolution Of Secondary Sexual Characters Research Articles

Evolutionary history of secondary sexual characters in the most species-rich genus of anurans, the direct-developing frogs of the genusPristimantis(Anura: Strabomantidae)

AbstractAncestral character-state reconstruction is a powerful method in phylogenetics that can be applied to elucidate the evolutionary history of secondary sexual characters. Here, we surveyed the variation and reconstructed the ancestral states of secondary sexual characters (i.e. sexual dichromatism, vocal slits and nuptial pads) for the most species-rich genus of anurans (Pristimantis) using maximum parsimony, maximum-likelihood and Bayesian methods. This study demonstrates that at least five independent transformation series account for the occurrence of sexual dichromatism in Pristimantis: dorsum, throat, venter, groin and posterior surface of thighs. The ancestral reconstructions suggest that the most recent common ancestor of Pristimantis lacks sexual dichromatism on these five body areas. Likewise, the occurrence of vocal slits and the absence of nuptial pads were inferred as ancestral conditions. Morphological synapomorphies were identified for Yunganastes and two infrageneric units within Pristimantis (the Pristimantis devillei and Pristimantis unistrigatus species groups). Our results demonstrate that the evolutionary history of the secondary sexual characters in Pristimantis followed a rather complex pattern of multiple independent gains and losses for which this genus is a promising model to investigate the evolution of secondary sexual characters in the context of the complex interactions between natural and sexual selection.

Reproductive competition and sexual selection.

This paper traces the development of our understanding of the development of different approaches to estimating the strength of reproductive competition and sexual selection in the two sexes, based on measures of the operational sex ratio, the opportunity for sexual selection and contrasts in selection gradients between the sexes. It argues that different approaches provide complementary insights into the causes of sex differences in reproductive competition, the operation of sexual selection and the evolution of secondary sexual characters and that improvements in our understanding of the evolution of secondary sexual characters will require a more comprehensive understanding of the ways in which social and ecological conditions modify reproductive competition and development in females and males.This article is part of the themed issue 'Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies'.

Quantifying mating success of territorial males and sneakers in a bower-building cichlid fish

The strategies and traits males evolve to mate with females are incredible in their diversity. Theory on the evolution of secondary sexual characters suggests that evolving any costly trait or strategy will pay off and stabilise in the population if it is advantageous compared to the alternative less costly strategy, but quantifying the relative success of the two can be difficult. In Lake Malawi, Africa, there are >200 species of cichlid fish in which the males form leks and spend several weeks per year building sand-castle “bowers” several times their size. We tested the idea that a less costly “sneaking” strategy could be successful by quantifying the mating success of bower-holding versus non-bower-holding males. We PIT-tagged every fish in a semi-natural experimental set-up and placed tag-readers on the side of bowers to determine which fish held a bower. We then genotyped the eggs removed from females’ mouths to assign paternity of each egg. Broods were fathered by up to 3 different males. Although paternity was mostly assigned to males that held a bower, a small number of males who did not own a bower were more successful than some of those that did, indicating a role for an alternative strategy in these bower builders.

Flight initiation distances in relation to sexual dichromatism and body size in birds from three continents

Predators exert strong selection pressures on their prey. Prey would therefore benefit by adjusting their behaviour to the risk of predation, while predators conversely would benefit from adjusting their behaviour to that of their prey. Extravagant ornamentation has evolved to attract mates and/or successfully compete with conspecifics of the same sex to secure high mating success, even if that occurs at a cost of increased risk of predation. Thus, sexually dichromatic species may be more susceptible to predation than sexually monochromatic species, and the presence of compensation is indicative of such species being more vulnerable. If extravagant ornamentation is costly in terms of predation risk, then we should expect sexually dichromatic species to have longer flight initiation distances (FID) than sexually monochromatic species. If ornamentation is acquired as a handicap with only individuals in prime condition being able to display with the smallest viability cost, we should expect sexually dichromatic individuals to have shorter FID than sexually monochromatic individuals. Such differences among individuals should, on an evolutionary time scale, translate into differences in FID being related to differences in sexual dichromatism among species. We investigated the relationship between FID and sexual dichromatism in phylogenetic analyses, while accounting for effects of continent (Australia, North America, and Europe), body mass, the interaction between sexual dichromatism and body mass and the interaction between sexual dichromatism and continent. In an analysis of 447 species we found shorter FID in sexually dichromatic than in sexually monochromatic species (consistent with the handicap hypothesis because sexually dichromatic species took greater risks), especially so at large body size. FID differed among continents and the relative difference in FID between sexually monochromatic and sexually dichromatic species was larger in Europe than in Australia and North America. These differences among continents may be attributed to latitudinal effects of predation. These findings are important for current ideas about the evolution of secondary sexual characters because they imply covarying continental differences in predation, especially for large bodied sexually dichromatic species.

Differential allocation in relation to mate song quality in the Bengalese finch

Postmating sexual selection plays an important part in the evolution of secondary sexual characters. Based on differential allocation theory that predicts biased reproductive investment of females depending on the attractiveness of mates, a number of previous studies have shown that egg production is related in various ways to ornamental sexual traits of males, but evidence for behavioural sexual traits is less abundant. In this study we examine such maternal effects in relation to birdsong. Because the Bengalese finch is a monomorphic songbird, courtship song serves a key role in mate choice. To take into account individual female differences in egg production performance, we sequentially paired naïve, captive, female Bengalese finches to two different males, and investigated if their reproductive investment (clutch size, egg mass and hatchling sex ratio) was related to the song traits of their mates. We found that clutch size and egg mass were highly repeatable within individual females while sex ratio was not. Despite the inflexibility of egg mass within each female, egg mass increased when females were mated to males with longer songs. In addition, we found a non-significant weak tendency toward male-biased sex ratio in relation to longer song duration of mates. Our findings suggest that females mated to better mates adjusted their reproductive investment by producing heavier eggs and possibly offspring of the more costly sex.

Male barn swallows use different signalling rules to produce ornamental tail feathers

The evolution of secondary sexual characters is the subject of controversial debate between those defending their role as ‘viability indicators’ and those arguing that ornaments are purely ‘attractive traits’ selected by females. Recent theoretical studies suggest that these hypotheses are not mutually exclusive, as both viability and attractiveness can contribute to improve the reproductive success of progeny and could thus simultaneously underlie female choices. If that is the case, strategies of cheaper advertisement, allowing the expression of larger ornaments for the same cost, could proliferate even in species in which honest signalling of viability prevails. Under this scenario, different males could invest a different amount of resources per ornament unit of expression, thus using different signalling rules. We studied the relationship between tail feather length (a trait that is the subject of a female mate preference) and feather mass (a measure of investment in feather production) in a barn swallow Hirundo rustica population. Different males used different and consistent signalling rules when developing ornamental feathers. That is, to produce a feather of a given length, each male used a constant amount of resources across different years, but this amount varied between males. Although the amount of material invested in feathers (feather mass) is a condition-dependent trait, the organization of this material in ornamental feathers (i.e. the signalling rules) was not. Neither survival nor risk of feather breakage was related to the signalling rules. Thus, these results suggest that both ‘viability’ and ‘runaway’ mechanisms are independent determinants of the evolution of ornamental sexual feathers in the barn swallow. A preference for long tails will ensure that females either obtain a sire with high viability, or one transferring the capability to produce longer and more attractive tails at a lower cost of production to its offspring.

Sexual Selection in Males and Females

Research on sexual selection shows that the evolution of secondary sexual characters in males and the distribution of sex differences are more complex than was initially suggested but does not undermine our understanding of the evolutionary mechanisms involved. However, the operation of sexual selection in females has still received relatively little attention. Recent studies show that both intrasexual competition between females and male choice of mating partners are common, leading to strong sexual selection in females and, in extreme cases, to reversals in the usual pattern of sex differences in behavior and morphology.

Phylogenetic relationships of antlered flies, Phytalmia Gerstaecker (Diptera: Tephritidae): the evolution of antler shape and mating behaviour

Abstract The genus Phytalmia (antlered flies, Diptera: Tephritidae) contains remarkable flies with elaborate male head projections known as antlers. The antlers are used in antagonistic intraspecific interactions between males competing to occupy oviposition sites. Phylogenetic relationships between the seven known species of Phytalmia were chosen to be investigated in order to determine the current monophyly of the genus and to assess the evolution of secondary sexual characters and associated behaviours, especially male antlers, fore‐femoral, spines and stilting. A phylogenetic analysis of Phytalmia was conducted using two closely related species from the same tribe (Phytalmiini): Sessilina nigrilinea (Walker) and Diplochorda minor Malloch, and one species from a different tribe (Dacini): the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) as outgroups. A total of 1259 base pairs of mitochondrial DNA (COII and 16S) and 35 morphological characters were included in the analysis, using parsimony and maximum likelihood inference methods. A phylogenetic tree generated from combined data was used to infer the evolution of antler shapes and associated behaviours in the genus. The results of this paper support the monophyly of Phytalmia, with P. cervicornis Gerstaecker the sister group of the remaining species. The phylogeny suggests a general decrease in antler complexity over evolutionary time; however, the behavioural sequence of male flies becomes more complex over time, with steps (e.g. stilting) being added to the repertoire during antagonistic encounters. Finally, there are strong correlations between functionally constrained morphological and behavioural characters, therefore allowing the authors to make predications for species whose behaviours are unknown based on morphological attributes and the authors' hypothesised evolution of Phytalmia.

Maternal immune factors and the evolution of secondary sexual characters

Secondary sexual characters have been hypothesized to reveal the ability of males to resist debilitating parasites. Although such reliable signaling of parasite resistance may be maintained by parasite-host coevolution, maternal effects potentially provide a previously neglected factor that could affect the level of genetic variation in resistance to parasites. That could be the case because maternal effects have an entirely environmental basis, or because they can maintain considerable amounts of genetic variation through epistatic effects, even in the presence of strong directional selection. Maternal effects have been shown to occur as maternal allocation of immune factors to offspring, and such allocation may depend on the mating prospects of sons, causing mothers to differentially allocate maternal effects to eggs in species subject to intense sexual selection. Here we show that a maternal effect through innate antibacterial immune defense, lysozyme, which is transferred from the mother to the egg in birds, is positively associated with the evolution of secondary sexual characters. Previous studies have shown that females differentially allocate lysozyme to their eggs when mated to attractive males, and elevated levels of lysozyme are associated with reduced hatching failure and superior health among neonates and adults. In this study, comparative analyses of lysozyme from eggs of 85 species of birds showed a strong positive relationship between brightness of male plumage and egg lysozyme, even when controlling for potentially confounding variables. These findings suggest that maternal immune factors may play a role in the evolution of secondary sexual characters.

Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): Systematics, morphology, and biogeography

The family Cervidae includes 40 species of deer distributed throughout the northern hemisphere, as well as in South America and Southeast Asia. Here, we examine the phylogeny of this family by analyzing two mitochondrial protein-coding genes and two nuclear introns for 25 species of deer representing most of the taxonomic diversity of the family. Our results provide strong support for intergeneric relationships. To reconcile taxonomy and phylogeny, we propose a new classification where the family Cervidae is divided in two subfamilies and five tribes. The subfamily Cervinae is composed of two tribes: the tribe Cervini groups the genera Cervus, Axis, Dama, and Rucervus, with the Père David’s deer ( Elaphurus davidianus) included in the genus Cervus, and the swamp deer ( Cervus duvauceli) placed in the genus Rucervus; the tribe Muntiacini contains Muntiacus and Elaphodus. The subfamily Capreolinae consists of the tribes Capreolini ( Capreolus and Hydropotes), Alceini ( Alces), and Odocoileini ( Rangifer + American genera). Deer endemic to the New World fall in two biogeographic lineages: the first one groups Odocoileus and Mazama americana and is distributed in North, Central, and South America, whereas the second one is composed of South American species only and includes Mazama gouazoubira. This implies that the genus Mazama is not a valid taxon. Molecular dating suggests that the family originated and radiated in central Asia during the Late Miocene, and that Odocoileini dispersed to North America during the Miocene/Pliocene boundary, and underwent an adaptive radiation in South America after their Pliocene dispersal across the Isthmus of Panama. Our phylogenetic inferences show that the evolution of secondary sexual characters (antlers, tusk-like upper canines, and body size) has been strongly influenced by changes in habitat and behaviour.

Ecology and evolution of extravagant feather ornaments

Abstract The ancestral conditions that permit the evolution of extravagant secondary sexual characters are of considerable theoretical and empirical interest because they allow identification of necessary ecological conditions, but also allow empirical tests of models of female mate preferences. We investigated the ancestral and derived state of a range of ecological and evolutionary variables that might have been implicated in the evolution of secondary sexual characters. Extravagant feather ornaments have evolved independently at least 70 times in birds, and the context of these evolutionary events was investigated statistically. The acquisition of feather ornaments was significantly associated with a change in social mating system from monogamy to polygyny or lekking. This association is consistent with the Fisherian mechanism of sexual selection. However, very often also the acquisition of feather ornaments occurred without change in mating system. Therefore, ornamentation can develop for reasons other than polygyny. We did not find any indication of male parental care, kind of food, foraging mode, coloniality, nest site, migration or body mass being significantly associated with a change in the state of ornamentation.

Comparative evidence for a positive correlation between haematozoan prevalence and mortality in waterfowl

AbstractHamilton and Zuk (1982) suggested a new hypothesis to explain the evolution of secondary sexual characters, namely that male ornaments may represent honest signals of male capacity to resist parasites. Since then several authors have addressed the question of the role played by parasites in the evolution of host secondary sexual characters. Comparative analyses of Hamilton and Zuk's hypothesis have, however, failed to show the predicted positive association between parasitism levels and sexually‐selected traits. One possible explanation for this discrepancy involves a low pathogenicity of the parasites used to test the hypothesis. Here we show that haemosporidians are positively correlated with mortality rates in a sample of waterfowl, and that the correlation between the two variables is of similar magnitude in both males and females. Contrary to the expectations based on the Hamilton and Zuk's hypothesis, we did not find any correlation between plumage brightness and haemosporidian prevalence. These results indicate that haemosporidians may have a pathogenic effect on their avian hosts and that plumage brightness is likely to have evolved in response to ecological factors other than parasitism infections.

Plumage Redness in Redpoll Finches Does Not Reflect Hemoparasitic Infection

An assumption of the Hamilton-Zuk model for the evolution of secondary sexual characters is that variation in the expression of these traits among conspecific individuals is a reliable indicator of their parasitic burden. Thus, if host-parasite coevolutionary processes are driving the evolution of sexual characters in a species, one expects to find a negative relationship between the exaggeration of sexual ornaments in a population of males and parasite prevalence or incidence. I analyzed hemoparasites in 97 breeding redpoll finches (Aves; Carduelinae; Carduelis f. flammea) caught at Churchill, Manitoba, in this context. Redpolls are small boreal passerines that show strong age and sexual dichromatism

Local Adaptation of the Tremadote Diplostomum phoxini to the European Minnow Phoxinus phoxinus, its Second Intermediate Host

In this paper we stress the important role that immature parasites can play in the interaction with their hosts and the importance of looking at juvenile hosts when studying parasite effects. These results are discussed in relation to the evolution of host-parasite associations and to Hamilton & Zuk's (1982) hypothesis on the evolution of secondary sexual characters. We exposed juvenile European minnows Phoxinus phoxinus from two lake populations to sympatric and allopatric Diplostomum phoxini in a reciprocal cross-infection experiment. Parasites from both localities were more infective to the sympatric hosts than to the allopatric ones. During the first 4 weeks after infection, when the parasites grow within the host, minnows from both sympatric host-parasite combinations grew less quickly than minnows infected with allopatric parasites

The effects of parasites on male ornaments and female choice in the lek-breeding black grouse (Tetrao tetrix)

We describe the results of two studies of parasitic infection in the black grouse (Tetrao tetrix). The first deals with our own observations of lekking black grouse in which the parasite levels of two blood parasites, the protozoan Leucocytozoon lovati and microfilaria, probably produced by a nematode worm Splendidofilaria tuvensis, were scored. We also obtained measures of age, survival, number of copulations, body mass and length of the ornamental tail feathers (the lyre) of the lekking males. The second study analysed the data from Lund (1954) which involved eight gut parasites obtained from birds which were killed. In the first study we found higher levels of infection of Leucocytozoon in adults relative to young birds. Parasites had no effect on male survival and there was no correlation in infection between the two types of parasites. Birds infected with microfilaria had shorter tail ornaments. There was no relationship between parasitic infection and mating success. However, the data indicated that such a trend indeed may exist for Leucocytozoon and the most successful males on the leks were less often infected by Leucocytozoon than other males. Results of the second study showed a negative relationship between parasite load (a combined measure of all parasites) and both ornamental tail feather length and body mass. These observations are compatible with, but not conclusive evidence for, the hypothesis of Hamilton and Zuk (1982) on the evolution of secondary sexual characters, where females choose to mate with genetically resistant males which show their resistance by expressing larger and more showy secondary sexual characters. Alternative explanations for the observed patterns are: females avoid infected males for some immediate benefit; and/or parasite loads are indicators of general stress rather than genetical resistance. Under the latter hypothesis females could mate with more vigorous males for reasons unrelated to parasite resistance.

Limited Female Choice and the Evolution of Secondary Sexual Characters

This article studies the role that limits on female mate choice in polygynous species play in the evolution of preferred secondary sexual traits. Analysis of a diploid model of evolution by female choice sexual selection that incorporates limited female choice shows that the conditions under which an allele coding for a novel secondary sexual trait will increase in frequency when rare are more restrictive when female choice is more limited. This suggests the prediction that, all else being equal, species or populations whose females have limited mate choice are less likely to be sexually dimorphic in secondary sexual traits compared to species or populations whose females have relatively less limited choice.

Reassessment of comparative evidence for Hamilton and Zuk theory on the evolution of secondary sexual characters

HAMILTON and Zuk1 proposed that elaborate secondary sexual characters may have evolved because they act as cues in mate choice by revealing the health of a potential mate. From this theory, they derived the prediction that species which are more liable to parasitic infection should possess well-developed secondary sexual characters. They went on to demonstrate a positive association between prevalence of haematozoa and plumage brightness across species of North American passerine birds. Subsequent analyses by one of us2 on the same colour data confirmed that the relationship with male brightness existed even when the effects of phylogenetic associations were taken into account. The relationship was also found across European passerines when behavioural and ecological correlates of colour and phytogeny were accounted for2. Here, using independently derived plumage brightness scores, we question these conclusions.

Evolution of Secondary Sexual Characters and Sexual Behavior Patterns in a Family of Viviparous Fishes (Cyprinodontiformes: Poeciliidae)

Aronson and Clark (1952) and Clark, Aronson and Gordon (1954) summarized the extensive behavioral work on these fishes, and they and Clark and Kamrin (1951) and Hubbs and Reynolds (1957) specifically studied the behavioral significance of fin and genitalic structure in Poeciliidae. Rosen and Gordon (1953) reviewed the mechanics of poeciliid genitalic and fin action in relation to copulatory motor patterns and provided an evolutionary interpretation of their findings. The present paper takes its origin from two separate reports, one behavioral and the other systematic3. It concerns the integration of structure and behavior in the evolution of the highly specialized, viviparous poeciliid fishes from a generalized, probably oviparous ancestor. The results of this study show, not unexpectedly, that the combination of comparative studies of behavior and functional anatomy may furnish insights on questions of evolution that do not emerge from either alone. The demonstrable effec-

Sexual Dimorphism in the Animal Kingdom; a Theory of the Evolution of Secondary Sexual Characters

HOWEVER much readers of this work may dissent from the views of the author, there can be no doubt that the volume is worthy of the most careful perusal. For the first time since the publication of Darwin's theory of sexual selection we have been provided with a bold and intelligible attempt at explaining secondary sexual characters on Lamarckian principles, and although many of us may arrive at the conclusion that Mr. Cunningham has not succeeded in establishing his case, it will be generally admitted that he has discussed the problem, on the whole, in a more or less scientific spirit, and has supported his arguments by a body of well-considered and, in many cases, original observations, which make his book exceptionally valuable as a storehouse of facts. Sexual Dimorphism in the Animal Kingdom; a Theory of the Evolution of Secondary Sexual Characters. By J. T. Cunningham Pp. xi + 317; with 32 illustrations. (London: Adam and Charles Black, 1900.)