Intraspecific variation in testis asymmetry in birds: evidence for naturally occurring compensation

In many taxa, the left and right testes often differ in size. The compensation hypothesis states that one testis of the pair serves as a ‘back-up’ for any reduced function in the other and provides a mechanism to explain intraspecific variation in degree and direction of gonad asymmetry. Although testis asymmetry is common in birds, evidence for natural testis compensation is unknown. Using a novel quantitative approach that can be applied to any bilateral organ or structure, we show that testis compensation occurs naturally in birds and can be complete when one testis fails to develop. Owing to a recurrent risk of testis impairment and an evolutionary trade-off between natural and sexual selections acting on the arrangement of internal organs in species with abdominal and/or seasonal testes, compensation adds an important, but neglected, dimension to measures of male reproductive investment.     

Testes asymmetry,condition and sexual selection in birds: an experimental test

The functional significance of the marked directional asymmetry in testes size observed in many bird species is obscure. Møller suggested that (i) the smaller of the two testes serves a compensatory role and increases in size (and hence reduces asymmetry) when the larger one is defective in some way, and (ii) as a consequence, the degree of directional asymmetry in testes size reflects male quality and covaries positively with the expression of secondary sexual traits. We conducted an experimental test of these two hypotheses in the zebra finch, Taeniopygia guttata. Neither hypothesis was supported. First, there was no significant relationship between the size of the left testis and relative testes asymmetry. Second, we obtained no support for the hypothesis that the degree of directional asymmetry in testes mass covaried with condition. On the contrary, directional asymmetry in testes mass was significantly greater in birds whose condition was experimentally reduced, compared with control birds. Moreover, we found no significant relationships between testes asymmetry and secondary sexual traits. We conclude that directional asymmetry in testes size does not reflect male condition in the zebra finch.     

No Evidence for the Compensation Hypothesis in the Swelled Vent Frog(Feirana quadranus)

The compensation hypothesis predicts that if the left testis is defective e.g. due to developmental stress,the increased right testis serves a compensatory role, and thereby displaying testes asymmetry which can be a reliable indicator of male body condition. Here, to test the prediction of the compensation hypothesis, we analyzed difference in size between left testis and right testis and the relationship between testes asymmetry and male body condition in the swelled vent frog(Feirana quadranus).We found that the left testis was larger than right testis,displaying a significant directional asymmetry in testes size. Although testes mass was correlated with body condition, testes asymmetry was not correlated with body condition, which cannot provide evidence that the right testis had a compensatory function. Our findings suggest no evidence for the compensation hypothesis in this species due to lacking the compensatory function in right testis.     

Behavioral and morphological asymmetries in chukar Alectoris chukar copulation

Birds often exhibit greater reproductive tract development on the left side than right side. Behavioral evidence from the three species for which data has been published indicates that these species copulate more frequently on the left side of females than on the right side. Missing from the literature are studies that compare asymmetry in copulation behavior to asymmetry in reproductive tract morphology of the same individuals of both sexes within a single species. To better understand the potential for cryptic sexual selection to influence avian copulation, we measured asymmetries in chukar Alectoris chukar copulation using 24 male and 29 female chukar brought into captivity from the wild. Chukar copulated (n=37) more from the left side (n=30) of females than the right side (n=7). The left testis of males was consistently greater in size, mass and volume than the right testis. The left ovary and oviduct of females was consistently functional with no observable development of the right ovary or oviduct. Left-side bias in direction of copulation, larger left testes, and functional left vaginal openings may act in concert to deliver spermatozoa to the oviduct, promoting fertilization.     

Testis asymmetry and sperm length in Rhacophorus omeimontis

Theory predicts that the degree of testes asymmetry should be positively correlated with male body condition in species with directional testis asymmetry. We tested this prediction in Rhacophorus omeimontis, a species in which females mate with more than one male. Our results showed that the treefrogs did not exhibit the absence of directional asymmetry in testis size, but rather the occurrence of fluctuating asymmetry. Moreover, we also tested differences in body size, body mass, testis mass, testis asymmetry, and sperm size among initially paired, jointly paired, and unpaired males. We found that body size and mass, testis mass, testis asymmetry and sperm length did not differ among the three male types. Testis mass showed a positive relationship with soma mass, but the correlations between the extent of fluctuating testis asymmetry and sperm length, and between testis mass and sperm length were not significant. Our data suggest that testes size and sperm length do not play an important role in determining male mating success in the presence of sperm competition.     

Left–right asymmetries and shape analysis on Ceroglossus chilensis (Coleoptera: Carabidae)

Bilateral symmetry is widespread in animal kingdom, however most animal can deviate from expected symmetry and manifest some kind of asymmetries. Fluctuating asymmetry is considered as a tool for valuating developmental instability, whereas directional asymmetry is inherited and could be used for evaluating evolutionary development. We use the method of geometric morphometrics to analyze left/right asymmetries in the whole body, in two sites and totally six populations of Ceroglossus chilensis with the aim to infer and explain morphological disparities between populations and sexes in this species. In all individuals analyzed we found both fluctuating asymmetry and directional asymmetry for size and shape variation components, and a high sexual dimorphism. Moreover a high morphological variability between the two sites emerged as well. Differences in diet could influence the expression of morphological variation and simultaneously affect body sides, and therefore contribute to the symmetric component of variation. Moreover differences emerged between two sites could be a consequence of isolation and fragmentation, rather than a response to local environmental differences between sampling sites.     

Left-right asymmetry of fly wings and the evolution of body axes.

The body plan of Drosophila, and presumably that of other insects, develops under the control of anterio-posterior and dorsal ventral axes, but no evidence for a left-right axis has yet been found. We used geometric morphometrics to study the wings in three species of flies: Drosophila melanogaster, Musca domestica and Glossina palpalis gambiensis. In all three species, we found that both size and shape showed subtle, but statistically significant directional asymmetry. For size, these asymmetries were somewhat inconsistent within and between species, but for shape, highly significant directional asymmetry was found in all samples examined. These systematic left-right differences imply the existence of a left-right axis that conveys distinct positional identities to the wing imaginal discs on either body side. Hence, the wing discs of Drosophila may be a new model to study the developmental genetics of left-right asymmetry. The asymmetries of shape were similar among species, suggesting that directional asymmetry has been evolutionarily conserved since the three lineages diverged. We discuss the implications of this evolutionary conservatism in conjunction with results from earlier studies that showed a lack of genetic variation for directional asymmetry in Drosophila.     

Shared pattern of endocranial shape asymmetries among great apes, anatomically modern humans, and fossil hominins

Anatomical asymmetries of the human brain are a topic of major interest because of their link with handedness and cognitive functions. Their emergence and occurrence have been extensively explored in human fossil records to document the evolution of brain capacities and behaviour. We quantified for the first time antero-posterior endocranial shape asymmetries in large samples of great apes, modern humans and fossil hominins through analysis of "virtual" 3D models of skull and endocranial cavity and we statistically test for departures from symmetry. Once based on continuous variables, we show that the analysis of these brain asymmetries gives original results that build upon previous analysis based on discrete traits. In particular, it emerges that the degree of petalial asymmetries differs between great apes and hominins without modification of their pattern. We indeed demonstrate the presence of shape asymmetries in great apes, with a pattern similar to modern humans but with a lower variation and a lower degree of fluctuating asymmetry. More importantly, variations in the position of the frontal and occipital poles on the right and left hemispheres would be expected to show some degree of antisymmetry when population distribution is considered, but the observed pattern of variation among the samples is related to fluctuating asymmetry for most of the components of the petalias. Moreover, the presence of a common pattern of significant directional asymmetry for two components of the petalias in hominids implicates that the observed traits were probably inherited from the last common ancestor of extant African great apes and Homo sapiens.These results also have important implications for the possible relationships between endocranial shape asymmetries and functional capacities in hominins. It emphasizes the uncoupling between lateralized activities, some of them well probably distinctive to Homo, and large-scale cerebral lateralization itself, which is not unique to Homo.     

A single functional testis and long deferent duct papillae: the peculiar male reproductive tract of the classically polyandrous, sex-role reversed Black Coucal (Centropus grillii)

In many birds, the male reproductive tract is asymmetric with the left testis being larger than the right one. Coucals (Centropodidae) represent an exception as the asymmetry is typically reversed. Here, we describe the functional morphology of the reproductive tract of the African Black Coucal (Centropus grillii), a bird species with reversed sex-roles and a classical polyandrous mating system. In this species, the left testis has been reduced to a tiny, disk-like vestige that in almost all cases examined was not visible macroscopically. The vestigial left testis apparently does not participate in sperm production but has retained a vestigial left excurrent duct system. By contrast, the right deferent duct was engorged with sperm, suggesting a sperm storage function. Both deferent ducts opened on the tip of spectacularly long, erectile deferent duct papillae into the urodaeum of the male cloaca. Behavioural observations suggest that they may function as “pseudophalli”. Testis mass represented 0.49% of body mass, less than half the size of other classical polyandrous bird species. Assuming moderate to high levels of sperm competition this represents a paradox. Heavy demands on the energy budget while caring for altricial young may have prevented males from maintaining two testes and large bilateral sperm storage devices. Reduced testis mass may be compensated for by frequent transfer of small amounts of sperm. Female Black Coucals have not evolved any corresponding cloacal specializations, but like all other birds have sperm storage tubules.     

Shared Pattern of Endocranial Shape Asymmetries among Great Apes,Anatomically Modern Humans,and Fossil Hominins

Anatomical asymmetries of the human brain are a topic of major interest because of their link with handedness and cognitive functions. Their emergence and occurrence have been extensively explored in human fossil records to document the evolution of brain capacities and behaviour. We quantified for the first time antero-posterior endocranial shape asymmetries in large samples of great apes, modern humans and fossil hominins through analysis of “virtual” 3D models of skull and endocranial cavity and we statistically test for departures from symmetry. Once based on continuous variables, we show that the analysis of these brain asymmetries gives original results that build upon previous analysis based on discrete traits. In particular, it emerges that the degree of petalial asymmetries differs between great apes and hominins without modification of their pattern. We indeed demonstrate the presence of shape asymmetries in great apes, with a pattern similar to modern humans but with a lower variation and a lower degree of fluctuating asymmetry. More importantly, variations in the position of the frontal and occipital poles on the right and left hemispheres would be expected to show some degree of antisymmetry when population distribution is considered, but the observed pattern of variation among the samples is related to fluctuating asymmetry for most of the components of the petalias. Moreover, the presence of a common pattern of significant directional asymmetry for two components of the petalias in hominids implicates that the observed traits were probably inherited from the last common ancestor of extant African great apes and Homo sapiens.These results also have important implications for the possible relationships between endocranial shape asymmetries and functional capacities in hominins. It emphasizes the uncoupling between lateralized activities, some of them well probably distinctive to Homo, and large-scale cerebral lateralization itself, which is not unique to Homo.     

Asymmetry pays: visual lateralization improves discrimination success in pigeons

Functional cerebral asymmetries, once thought to be exclusively human, are now accepted to be a widespread principle of brain organization in vertebrates [1]. The prevalence of lateralization makes it likely that it has some major advantage. Until now, however, conclusive evidence has been lacking. To analyze the relation between the extent of cerebral asymmetry and the degree of performance in visual foraging, we studied grain-grit discrimination success in pigeons, a species with a left hemisphere dominance for visual object processing [2,3]. The birds performed the task under left-eye, right-eye or binocular seeing conditions. In most animals, right-eye seeing was superior to left-eye seeing performance, and binocular performance was higher than each monocular level. The absolute difference between left- and right-eye levels was defined as a measure for the degree of visual asymmetry. Animals with higher asymmetries were more successful in discriminating grain from grit under binocular conditions. This shows that an increase in visual asymmetry enhances success in visually guided foraging. Possibly, asymmetries of the pigeon's visual system increase the computational speed of object recognition processes by concentrating them into one hemisphere while preventing the other side of the brain from initiating conflicting search sequences of its own.     

Rhodnius prolixus and Rhodnius robustus–like (Hemiptera, Reduviidae) wing asymmetry under controlled conditions of population density and feeding frequency

Habitat change in Rhodnius spp may represent an environmental challenge for the development of the species, particularly when feeding frequency and population density vary in nature. To estimate the effect of these variables in stability on development, the degree of directional asymmetry (DA) and fluctuating asymmetry (FA) in the wing size and shape of R. prolixus and R. robustus–like were measured under laboratory controlled conditions. DA and FA in wing size and shape were significant in both species, but their variation patterns showed both inter-specific and sexual dimorphic differences in FA of wing size and shape induced by nutrition stress. These results suggest different abilities of the genotypes and sexes of two sylvatic and domestic genotypes of Rhodnius to buffer these stress conditions. However, both species showed non-significant differences in the levels of FA between treatments that simulated sylvan vs domestic conditions, indicating that the developmental noise did not explain the variation in wing size and shape found in previous studies. Thus, this result confirm that the variation in wing size and shape in response to treatments constitute a plastic response of these genotypes to population density and feeding frequency.     

Sperm competition and the evolution of testes size in birds

Comparative analyses suggest that a variety of ecological and behavioural factors contribute to the tremendous variability in extrapair mating among birds. In an analysis of 1010 species of birds, we examined several ecological and behavioural factors in relation to testes size; an index of sperm competition and the extent of extrapair mating. In univariate and multivariate analyses, testes size was significantly larger in species that breed colonially than in species that breed solitarily, suggesting that higher breeding density is associated with greater sperm competition. After controlling for phylogenetic effects and other ecological variables, testes size was also larger in taxa that did not participate in feeding their offspring. In analyses of both the raw species data and phylogenetically independent contrasts, monogamous taxa had smaller testes than taxa with multiple social mates, and testes size tended to increase with clutch size, which suggests that sperm depletion may play a role in the evolution of testes size. Our results suggest that traditional ecological and behavioural variables, such as social mating system, breeding density and male parental care can account for a significant portion of the variation in sperm competition in birds.     

The evolution of egg shape in birds: selection during the incubation period

A recent broad comparative study suggested that factors during egg formation – in particular ‘flight efficiency’, which explained only 4% of the interspecific variation – are the main forces of selection on the evolution of egg shape in birds. As an alternative, we tested whether selection during the incubation period might also influence egg shape in two taxa with a wide range of egg shapes, the alcids (Alcidae) and the penguins (Spheniscidae). To do this, we analysed data from 30 species of these two distantly related but ecologically similar bird families with egg shapes ranging from nearly spherical to the most pyriform eggs found in birds. The shape of pyriform eggs, in particular, has previously proven difficult to quantify. Using three egg‐shape indices – pointedness, polar‐asymmetry and elongation – that accurately describe the shapes of all birds’ eggs, we examined the effects of egg size, chick developmental mode, clutch size and incubation site on egg shape. Linear models that include only these factors explained 70–85% of the variation in these egg‐shape indices, with incubation site consistently explaining > 60% of the variation in shape. The five species of alcids and penguins that produce the most pyriform eggs all incubate in an upright posture on flat or sloping substrates, whereas species that incubate in a cup nest have more spherical eggs. We suggest that breeding sites and incubation posture influence the ability of parents to manipulate egg position, and thus selection acting during incubation may influence egg‐shape variation across birds as a whole.     

Effect of composition on shape of bird eggs

Numerous studies over the past 90 years have described the various bird egg shapes in mathematical terms but few studies have considered the underlying reasons for such interspecific egg shape variability. This study investigated how the size and composition, i.e. proportions of shell, yolk and albumen, were associated with egg shape. Geometric morphometrics were used to generate principal components, which were analysed in relation to taxonomy (i.e. avian order) and degree of neonatal developmental maturity, which correlates with egg composition. The analysis confirmed previous results that most of the variation in shape is associated with degree of elongation (i.e. length divided by breadth) and asymmetry (i.e. position of the broadest part of the egg away from the mid‐point of the egg's length). Egg shape reflected avian order but not developmental maturity. The degree of elongation of an egg is related to absolute egg mass and the proportion of yolk. By contrast, the degree of asymmetry is related to the proportion of shell and the mass of the egg relative to female body mass. Although significant, the models explained little of the variation in egg shape and so it was concluded that other factors, such as pelvis size and shape, could be more important in determining egg shape in birds.     

Using testis size to predict the mating systems of New Zealand geckos

Abstract

The mating system is unknown for the majority of New Zealand geckos (Family Gekkonidae). I investigated interspecific variation in relative testis volume across 19 New Zealand gecko taxa and 63 additional species of squamate reptiles from other countries to make predictions about the social mating system of the New Zealand geckos. Relative testis size varied greatly between species of New Zealand gecko, with testes ranging from 119% larger than expected to 75% smaller than expected. This variation was even greater across other squamates, with testes ranging from 55 to 152% of expected size. This variation could not be explained by seasonality of breeding, clutch size or the sex ratio of populations. As species subject to more intense sperm competition sport relatively larger testes in other vertebrate groups, it is likely that similar variation in gecko testis size is due to differences in mating systems between species. Based on testis volume, it is predicted that at least half of the New Zealand gecko taxa studied are likely to have polygynandrous mating systems.     

Larger testes are associated with a higher level of polyandry, but a smaller ejaculate volume, across bushcricket species (Tettigoniidae)

While early models of ejaculate allocation predicted that both relative testes and ejaculate size should increase with sperm competition intensity across species, recent models predict that ejaculate size may actually decrease as testes size and sperm competition intensity increase, owing to the confounding effect of potential male mating rate. A recent study demonstrated that ejaculate volume decreased in relation to increased polyandry across bushcricket species, but testes mass was not measured. Here, we recorded testis mass for 21 bushcricket species, while ejaculate (ampulla) mass, nuptial gift mass, sperm number and polyandry data were largely obtained from the literature. Using phylogenetic-comparative analyses, we found that testis mass increased with the degree of polyandry, but decreased with increasing ejaculate mass. We found no significant relationship between testis mass and either sperm number or nuptial gift mass. While these results are consistent with recent models of ejaculate allocation, they could alternatively be driven by substances in the ejaculate that affect the degree of polyandry and/or by a trade-off between resources spent on testes mass versus non-sperm components of the ejaculate.     

Functional infertility among territorial males in two passerine species, the willow warbler Phylloscopus trochilus and the bluethroat Luscinia svecica

Information about male infertility in free-living birds is scarce, but anecdotal and circumstantial evidence suggests that it does occur regularly at a low frequency. In this paper we document three cases of azoospermia in two passerine species, the willow warbler Phylloscopus trochilus and the bluethroat Luscinia svecica at their breeding grounds in South Norway. In willow warblers, two males out of a sample of 50 territory holders had no sperm in their seminal glomera, the storage site of sperm ready for ejaculation. The two males also had very small testes. One out of 48 bluethroat males also had no sperm in the seminal glomera. This male had an extreme asymmetry of the testes, with the right testis being about twice as large as the left. He also failed to fertilize any eggs in his own nest, as well as in neighbouring nests, as revealed by microsatellite genotyping. Thus, the proportion of males without sperm seems to be at a magnitude of a few (2–4) percent in both species. These are among the first estimates of the frequency of azoospermia in wild birds. Our results indicate a significant risk for sexually monogamous females of laying unfertilized eggs, which could favour the evolution of extra-pair copulation as a fertility insurance strategy in females.     

SPERM COMPETITION SELECTS BEYOND RELATIVE TESTES SIZE IN BIRDS

Sperm morphology varies considerably across taxa, and postcopulatory sexual selection is thought to be one of the main forces responsible for this diversity. Several studies have investigated the effects of the variation in sperm design on sperm function, but the consequences of variation in sperm design on testis morphology have been overlooked. Testes size or architecture may determine the size of the sperm they produce, and selection for longer sperm may require concomitant adaptations in the testes. Relative testes size differs greatly between species and is often used as an index of sperm competition, but little is known about whether larger testes have more sperm-producing tissue or produce sperm at a faster rate. Using a comparative approach in New World Blackbirds (Icteridae), we found (1) a strong link between testis histology and sperm length, suggesting selection on testis architecture through selection on sperm size, and (2) that species under intense sperm competition had a greater proportion of sperm-producing tissue within their testes. These results support the prediction that sperm competition fosters adaptations in reproductive organs that extend beyond testes size, and raise questions about the trade-offs influencing reproductive investment.     

Quantitative-genetic analysis of wing form and bilateral asymmetry in isochromosomal lines ofDrosophila subobscura using Procrustes methods

Fluctuating asymmetry (FA) is often used as a measure of underlying developmental instability (DI), motivated by the idea that morphological variance is maladaptive. Whether or not DI has evolutionary potential is a highly disputed topic, marred by methodological problems and fuzzy prejudices. We report here some results from an ongoing study of the effects of karyotype, homozygosity and temperature on wing form and bilateral asymmetry using isochromosomal lines ofDrosophila subobscura. Our approach uses the recently developed methodologies in geometric morphometrics to analyse shape configurations of landmarks within the standard statistical framework employed in studies of bilateral asymmetries, and we have extended these methods to partition the individual variation and the variation in asymmetries into genetic and environmental causal components. The analyses revealed temperaturedependent expression of genetic variation for wing size and wing shape, directional asymmetry (DA) of wing size, increased asymmetries at suboptimal temperature, and a transition from FA to DA in males as a result of increase in the rearing temperature. No genetic variation was generally detected for FA in our samples, but these are preliminary results because no crosses between lines were carried out and, therefore, the contribution of dominance was not taken into account. In addition, only a subset of the standing genetic variation was represented in the experiments.