Variation In Testis Size Research Articles

Measuring mantled howler monkey (Alouatta palliata) testes via parallel laser photogrammetry: Expanding the use of noninvasive methods.

Parallel laser photogrammetry (PLP), which consists of attaching two or three parallel laser beams at a known inter-beam distance to a camera, can be used to collect morphological measurements of organisms noninvasively. The lasers project onto the photo being taken, and because the inter-beam distance is known, they act as a scale for image analysis programs like ImageJ. Traditionally, this method has been used to measure larger morphological traits (e.g., limb length, crown-rump length) to serve as proxies for overall body size, whereas applications to smaller anatomical features remain limited. To that end, we used PLP to measure the testes of 18 free-living mantled howler monkeys (Alouatta palliata) at La Selva Biological Station, Costa Rica. We tested whether this method could reliably measure this relatively small and globular morphology, and whether it could detect differences among individuals. We tested reliability in three ways: within-photo (coefficient of variation [CV] = 4.7%), between-photo (CV = 5.5%), and interobserver (intraclass correlation = 0.92). We found an average volume of 36.2 cm3 and a range of 16.4-54.4 cm3, indicating variation in testes size between individuals. Furthermore, these sizes are consistent with a previous study that collected measurements by hand, suggesting that PLP is a useful method for making noninvasive measurements of testes.

Testis Size Variation and Its Environmental Correlates in Andrew's Toad (Bufo andrewsi).

Reproductive investments influenced by environmental conditions vary extensively among geographically distinct populations. However, investigations of patterns of intraspecific variation in male reproductive investments and the mechanisms shaping this variation in anurans remain scarce. Here, we focused on the variation in testis size in 14 populations of the Andrew's toad Bufo andrewsi, a species with weak dispersal ability but wide distribution in southwestern China, to establish whether male reproductive investment varies on an environmental gradient. Our analysis revealed a significant variation in relative testis size across populations, and a positive correlation between testis size and body condition. We, however, found no geographic trends explaining the variability in the testis size. The relative testis size did not increase with increasing latitude or altitude. We also found no relationship between relative testis size and rainfall, but a negative correlation with the coefficient of variation of temperature, with larger testes under stable environments. These findings suggest that the decreased male reproductive investment of this species may be a consequence of harsher or fluctuating environmental conditions.

The spatial and temporal distribution of females influence the evolution of testes size in Australian rodents.

Male-male competition after mating (sperm competition) favours adaptations in male traits, such as elevated sperm numbers facilitated by larger testes. Ultimately, patterns of female distribution will affect the strength of sperm competition by dictating the extent to which males are able to prevent female remating. Despite this, our understanding of how the spatial and temporal distributions of mating opportunities have shaped the evolutionary course of sperm competition is limited. Here, we use phylogenetic comparative methods to explore interspecific variation in testes size in relation to patterns of female distribution in Australian rodents. We find that as mating season length (temporal distribution of females) increases, testes size decreases, which is consistent with the idea that it is difficult for males to prevent females from remating when overlap among oestrous females is temporally concentrated. Additionally, we find that social species (spatially clustered) have smaller testes than non-social species (spatially dispersed). This result suggests that males may be effective in monopolizing reproduction within social groups, which leads to reduced levels of sperm competition relative to non-social species where free-ranging females cannot be controlled. Overall, our results show that patterns of female distribution, in both space and time, can influence the strength of post-mating sexual selection among species.

TESTIS ABNORMALITIES IN A POPULATION OF SOUTH AUSTRALIAN KOALAS (PHASCOLARCTOS CINEREUS).

Testis asymmetry, in which the testes in an individual differ in size, has recently been reported in koalas (Phascolarctos cinereus) in the Mount Lofty Ranges population of South Australia. We describe the morphology and histology of both testes from affected individuals in this population (n=56) and the parameters of koalas with normal-sized testes based on age and breeding season (n=56). Morphologic measurements included testis weight, length, width, and volume; histologic parameters included seminiferous tubule diameter, seminiferous epithelial height, and seminiferous tubule (interstitial tissue ratio and presence or absence of spermatozoa). Of the 56 koalas with intraindividual variation in testes size, 47 were classified as asymmetric and nine as microtestes. For koalas with asymmetric testes, all morphologic parameters were significantly decreased in the smaller testes compared with normal-sized testes, but for the histologic parameters, only seminiferous tubule diameter was significantly less. Histopathologic examination of the asymmetric testes showed 38 with normal parenchyma histologically indistinguishable between intraindividual testes, four with degeneration and atrophy, and three with hypoplasia, whereas examination of microtestes showed degeneration and atrophy in seven, hypoplasia in one, and aplasia in one. No association of testis size difference with Chlamydia pecorum infection was found in a subset of animals. For the 56 koalas with normal-sized testes, morphologic parameters were found to increase with age, and juvenile and young adults were found to have smaller seminiferous tubule diameters than adults. No differences were found between testes of koalas in the breeding and nonbreeding season. Overall, these findings indicate that testis asymmetry in koalas from the Mount Lofty Ranges population is common but not associated with decreased function, except where testis malformations such as hypoplasia or aplasia occur or when parenchyma has been disrupted by acquired disease.

In Search of an Honest Butterfly: Sexually Selected Wing Coloration and Reproductive Traits From Wild Populations of the Cabbage White Butterfly

Abstract Sexual selection is central to many theories on mate selection and individual behavior. Relatively little is known, however, about the impacts that human-induced rapid environmental change are having on secondary sexually selected characteristics. Honest signals function as an indicator of mate quality when there are differences in nutrient acquisition and are thus potentially sensitive to anthropogenically altered nutrient inputs. We used the cabbage white butterfly, Pieris rapae (L.) (Lepidoptera: Pieridae), to investigate differences in color and testes size in a system that is often exposed to agricultural landscapes with nitrogen addition. We collected individuals from four sites in California and Nevada to investigate variation in key traits and the possibility that any relationship between wing color and a reproductive trait (testes size) could vary among locations in the focal butterfly. Coloration variables and testes size were positively albeit weakly associated across sites, consistent with the hypothesis that females could use nitrogen-based coloration in the cabbage white as an indicator for a male mating trait that has the potential to confer elevated mating success in progeny. However, variation in testes size and in the relationship between testes size and wing color suggest complexities that need exploration, including the possibility that the signal is not of equal value in all populations. Thus these results advance our understanding of complex relationships among environmental change and sexual selection in the wild.

Extensive geographical variation in testes size and ejaculate traits in a terrestrial-breeding frog.

Ejaculate traits vary extensively among individuals and species, but little is known about their variation among populations of the same species. Here, we investigated patterns of intraspecific variation in male reproductive investment in the terrestrial-breeding frog Pseudophryne guentheri. Like most anurans, breeding activity in P. guentheri is cued by precipitation, and therefore the timing and duration of breeding seasons differ among geographically separated populations, potentially leading to differences in the level of sperm competition. We, therefore, anticipated local adaptation in sperm traits that reflect these phenological differences among populations. Our analysis of six natural populations across a rainfall gradient revealed significant divergence in testes and ejaculate traits that correspond with annual rainfall and rainfall seasonality; males from the northern and drier edge of the species range had significantly smaller testes containing fewer, smaller and less motile sperm compared with those from mesic central populations. These findings may reflect spatial variation in the strength of postcopulatory sexual selection, likely driven by local patterns of precipitation.

Extreme variation in testes size in an insect is linked to recent mating activity.

Ample sperm production is essential for successful male reproduction in many species. The amount of sperm a male can produce is typically constrained by the size of his testes, which can be energetically expensive to grow and maintain. Although the economics of ejaculate allocation has been the focus of much theoretical and empirical literature, relatively little attention has been paid to individual adult variation and plasticity at the source of sperm production, the testes themselves. We experimentally address this issue using the insect Narnia femorata Stål (Hemiptera: Coreidae). We established the metabolic cost of testicular tissue and then quantified variation in individual testes mass in response to multiple mate quality and quantity treatments. We uncovered extreme variation across individuals and considerable short-term effects of mating activity on testes dry mass. Importantly, the observed variation in testes mass was associated with notable fitness consequences; females paired with males with larger testes had greater hatching success. Overall, pairing with a female resulted in a 11% reduction in dry testes mass. Despite this apparent considerable mating investment, we found no evidence of strategic allocation to higher quality females or longer-term changes in testes mass. The dynamic nature of testes mass and its metabolic cost is vital to consider in the context of re-mating rates, polyandry benefits and general mating system dynamics both in this species and more broadly.

Testes mass in the livebearing fish Brachyrhaphis rhabdophora (Poeciliidae) varies hypoallometrically with body size but not between predation environments.

In this study, we considered potential causes of variation in testis size in the livebearing fish Brachyrhaphis rhabdophora. We evaluated variation in testes mass among individual males and among populations that occupy different selective environments. First, we predicted that small males should allocate more to testes mass than large males (i.e., hypoallometric pattern) based on a sperm competition argument. Second, based on life history theory and associated differences in mortality rates between populations that coexist with many fish predators and those with few predators, we predicted that males in high‐predation environments should allocate more to testes mass than males in habitats with few predators. Our results showed that small males allocated proportionally more to testes mass than larger males (slope of testes mass to body mass was hypoallometric). However, there was no effect of predator environment on testes mass independent of body size differences. In this system, size‐specific patterns of reproductive allocation in males (hypoallometry) differ from that seen in females (hyperallometry). Allocation to testes mass may respond to differences in mortality rate through selection on body size.

Failed sperm development as a reproductive isolating barrier between species.

Hybrid male sterility is a common reproductive isolating barrier between species. Yet, little is known about the actual developmental causes of this phenomenon, especially in naturally hybridizing species. We sought to evaluate the developmental causes of hybrid male sterility, using spadefoot toads as our study system. Plains spadefoot toads (Spea bombifrons) and Mexican spadefoot toads (S. multiplicata) hybridize where they co-occur in the southwestern USA. Hybrids are viable, but hybrid males suffer reduced fertility. We compared testes size and developmental stages of sperm cell maturation between hybrid males and males of each species. We found that testes of hybrid males did not differ in mean size from pure-species males. However, hybrids showed a greater range of within-individual variation in testes size than pure-species males. Moreover, although hybrids produced similar numbers of early stage sperm cells, hybrids produced significantly fewer mature spermatozoids than pure-species males. Interestingly, an introgressed individual produced numbers of live sperm comparable to pure-species males, but the majority of these sperm cells were abnormally shaped and non-motile. These results indicate that hybrid incompatibilities in late sperm development serve as a reproductive isolating barrier between species. The nature of this breakdown highlights the possibilities that hybrid males may vary in fertility and that fertility could possibly be recovered in introgressed males.

Among-population covariation between sperm competition and ejaculate expenditure in frogs

Sperm competition theory predicts that among populations and species, male expenditure on the ejaculate should increase with the strength of selection from sperm competition, a prediction for which there is strong evidence from comparative studies of a variety of taxa. Patterns of geographic variation within species can provide important insights into adaptive coevolution; yet, few studies have adopted this approach in studying adaptation to sperm competition. We used highly polymorphic microsatellite markers to genotype clutches of eggs sampled from each of 10 populations across the geographic range of the Australian myobatrachid frog Crinia georgiana. The proportion of clutches with mixed paternity ranged from 0.27 to 0.60. We found significant among-population variation in testes size, the number of sperm stored within the testes, and in the proportion of sperm that were motile. A significant proportion of the among-population variation in testes size and number of sperm was predicted by variation in the density of breeding males found within populations. The covariation between male breeding density and ejaculate expenditure we have found within C. georgiana could be explained either by phenotypic plasticity in ejaculate expenditure in response to local variation in sperm competition risk or an evolutionary divergence in ejaculate expenditure among populations that is driven by variation in the strength of selection from sperm competition. Both scenarios are consistent with sperm competition theory. Key words: geographic variation, sperm competition risk, sperm quality, testis size. [Behav Ecol]

Sperm competition and sperm length influence the rate of mammalian spermatogenesis

Sperm competition typically favours an increased investment in testes, because larger testes can produce more sperm to provide a numerical advantage in competition with rival ejaculates. However, interspecific variation in testis size cannot be equated directly with variation in sperm production rate--which is the trait ultimately selected under sperm competition--because there are also differences between species in the proportion of spermatogenic tissue contained within the testis and in the time it takes to produce each sperm. Focusing on the latter source of variation, we provide phylogenetically controlled evidence for mammals that species with relatively large testes (and hence a high level of sperm competition) have a shorter duration of the cycle of the seminiferous epithelium and consequently a faster rate of spermatogenesis, enabling males to produce more sperm per unit testis per unit time. Moreover, we identify an independent negative relationship between sperm length and the rate of spermatogenesis, such that spermatogenesis takes longer in species with longer sperm. We conclude that sperm competition selects for both larger testes and a faster rate of spermatogenesis to increase overall sperm production, and that an evolutionary trade-off between sperm size and numbers may be mediated via constraints on the rate of spermatogenesis imposed by selection for longer sperm.

Cooperative Breeding in Groups of Synchronously Mating Females and Evolution of Large Testes to Avoid Sperm Depletion in African Striped Mice1

Testis size has been related to the mating system of both vertebrates and invertebrates. These differences are regarded as adaptive responses to sperm competition in promiscuously mating species. However, not all variation in testis size can be explained by sperm competition. Here, we test the hypothesis that the evolution of large testes occurs when synchronously breeding females must be fertilized within a short period of time to avoid reproductive competition among the females. African striped mouse (Rhabdomys pumilio) males of a polygynous population with cooperative breeding and high risk of sperm depletion had testes and cauda epididymis twice as large as those of males of four different promiscuous populations with high risk of sperm competition. When paired with three females simultaneously in captivity, males of the polygynous population bred with three females within 8 days, leading to synchronous births in their harems, thereby potentially reducing the risk of infanticide. Males from the promiscuous population reproduced with only one or two females within 8 days, and births were not synchronous. We conclude that large testes are selected for in species with synchronously mating females, which is ultimately beneficial for the evolution of cooperative breeding.

Does Testis Size in Cuckoos Vary with Paternal Care?

Abstract.— Male birds confront a tradeoff between increasing the number of offspring they sire and providing parental care. This behavioral tradeoff may be manifested as variation in testis size: larger testes, producing more sperm and testosterone, are advantageous for sperm and mating competition, thus ensuring paternity, yet high levels of plasma testosterone also inhibit parental care. There is good evidence that relative testis size is greater in species in which males compete more intensely to fertilize females, but it remains unclear whether, in turn, smaller testes prevail in species with greater levels of paternal care. Cuckoos provide an opportunity to test for an effect of paternal care on testis size because of the diversity of breeding systems in this family: parasitic species lack parental care altogether, whereas some coucals (Centropodinae) show exclusively or predominantly male care. In addition, coucals have a reduced left testis, which Ligon (1997) suggested may promote male care. We te...

The frequency of multiple paternity predicts variation in testes size among island populations of house mice

Polyandry generates selection on males through sperm competition, which has broad implications for the evolution of ejaculates and male reproductive anatomy. Comparative analyses across species and competitive mating trials within species have suggested that sperm competition can influence the evolution of testes size, sperm production and sperm form and function. Surprisingly, the intraspecific approach of comparing among population variation for investigating the selective potential of sperm competition has rarely been explored. We sampled seven island populations of house mice and determined the frequency of multiple paternity within each population. Applying the frequency of multiple paternity as an index of the risk of sperm competition, we looked for selective responses in male reproductive traits. We found that the risk of sperm competition predicted testes size across the seven island populations of house mice. However, variation in sperm traits was not explained by sperm competition risk. We discuss these findings in relation to sperm competition theory, and other intrinsic and extrinsic factors that might influence ejaculate quality.

Testis size depends on social status and the presence of male helpers in the cooperatively breeding cichlid Julidochromis ornatus

Cooperatively breeding animals, in which helpers may participate in reproduction with dominant breeders, are ideal species for examining intraspecific variation in testis size because they often exhibit both monogamous breeding (low risk of sperm competition) and polyandrous breeding (high risk) within a population. However, little is known about testis investment as a result of sperm competition in these animals. The substrate-brooding cichlid fish Julidochromis ornatus has a cooperatively breeding system, in which some males mate monogamously and other males reproduce as dominant breeders or helpers within cooperatively breeding groups, in which male helpers frequently sire young. We examined the relationship between testis investment and male social status in relation to the risk of sperm competition. As predicted from sperm competition models, in groups with male helpers, both the male breeders and the male helpers invested more in testes mass, compared to breeding males without male helpers. We also found a positive relationship between the testes mass of male breeders and their male helpers, suggesting that males increase their investment in reproductive capability under the risk of sperm competition. Sperm competition models also predict that larger testes are associated with increased siring success. Our paternity analysis supported this prediction; we found a positive relationship between testis investment by male helpers and the number of offspring they sired.

Bigger testes do work more: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp.

Evolutionary theory predicts that more resources are allocated to sperm production when sperm competition is high. This prediction is supported by both comparative and experimental data on static measures of male allocation, such as testis and ejaculate size. However, resource allocation is a dynamic process, and it is therefore important to evaluate if the static measures reflect this. Such an evaluation has to our knowledge never been done. Immunocytochemical labelling with bromodeoxyuridine (BrdU) allows visualisation of cells in S-phase. BrdU becomes incorporated into cells if, and only if, they are actively undergoing DNA duplication, which is a dynamic process. The number of BrdU-positive cells in the testis can hence serve as a dynamic measure of male allocation, i.e. testicular activity. We evaluate the relationship between testis size and testicular activity in the marine flatworm Macrostomum sp. In a previous study, we showed that testis size is phenotypically plastic in this species, and that worms make larger testes when they are raised in larger groups. We use this plasticity to experimentally produce variation in testis size, and demonstrate that larger testes are associated with higher testicular activity. Moreover, testis size and testicular activity were related linearly. We have thus, for the first time, shown that testis size is a good measure of resource allocation to the male function. Moreover, increased testicular activity is probably one of the first steps in the upregulation of sperm production. It is thus expected that testicular activity is a more sensitive measure of short-term variation in male allocation than the commonly used static measures.

Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk ( Tamias amoenus ): implications for sperm competition and reproductive success

Comparative analyses have found that relative testis size is a strong predictor of the prevalence of sperm competition for many taxa, including mammals, yet underlying this pattern is the assumption that intraspecific variation in testis size is related to individual fitness. Because intraspecific variation in ejaculate investment underlies interspecific patterns, it is critical to understand the causes and consequences of intraspecific variation in ejaculate investment. We examined relationships between ejaculate investment (testis size and sperm length) and reproductive success, body size and condition in the yellow-pine chipmunk (Tamias amoenus), a small ground squirrel in which sperm competition occurs. We examined genetic estimates of male reproductive success from a wild population of yellow-pine chipmunks and determined that males with large testes had higher annual reproductive success than males with small testes. This result provides empirical support for the numerous comparative studies that indicate testis size is associated with the intensity of sperm competition. In addition, males in good condition had relatively larger testes than males in poor condition, but there was no evidence of sperm length being dependent on condition. Finally, contrary to many predictions, males that invested more in sperm production (relatively heavy testes) produced shorter sperm, not longer sperm, than males that invested less.

Intraspecific variation in testis size of small mammals: implications for muscle mass

Intraspecific variation in testis size is usually interpreted in the context of sperm competition, yet an unconsidered consequence of increased testis size may be an increase in the production of testosterone, which can affect the growth of muscle mass. After muscle mass is corrected for body size, male small mammals have more muscle mass than females, which suggests that it may be a sexually selected trait. An enhanced musculature may have fitness consequences with respect to male mate-searching activities and male–male competition for access to females. We tested the prediction that males with large testes have more muscle mass (measured as lean dry mass) by examining testis size and body composition in three species of small mammals (bushy-tailed wood rat (Neotoma cinerea), deer mouse (Peromyscus maniculatus), and red-backed vole (Clethrionomys gapperi)) from the Kananaskis Valley, Alberta. In all three species, males with relatively large testes had relatively more lean dry mass than males with relatively small testes. This suggests that a secondary consequence of relatively large testes may be a relative increase in muscle mass. Further research should investigate alternative effects of intraspecific variation in testis size on individual fitness within wild populations to gain further insight into sexual selection.

Male wrens with large testes breed early

To display to females, male wrens, Troglodytes troglodytes, use cock nests built on their territories. Nest building starts about a month before the first females begin egg laying. The timing of nest building is highly variable between males with up to 8 weeks separating the earliest from the latest males to initiate this display activity. Males that weigh more before the breeding season initiate nest building earlier than lighter males. We measured testis size in male wrens in the prebreeding period during which seasonal testicular recrudescence is occurring. The initiation of nest building was predicted by male age and by testis size. This suggests that variation in the start of courtship activity may reflect variation between males in the rate of testicular recrudescence. Variation in male prebreeding body mass was influenced by variation in testis size, which suggests that the relation reported earlier between body mass and timing of nest construction could be explained, in part, by variation in testis size. Alternatively, if body mass reflects body condition then both the extent of testes recrudescence and the timing of courtship activity could be condition-dependent traits.

Testis size variation in the greenfinch Carduelis chloris : relevance for some recent models of sexual selection

Interspecific evidence that testis size responds to selection caused by sperm competition has been obtained from many taxa. However, little is known about the sources of intraspecific variation in testis size, although such variation may have functional significance. Variation in testis size and asymmetry was studied within and between eight geographically separated (and genetically differentiated) populations of greenfinches Carduelis chloris. The relationships between testis size and plumage brightness (degree of yellowness) and the prevalence of haematozoan infections were also investigated in three of these populations, as they related to the predictions of the immunocompetence handicap hypothesis, and Moller's hypothesis relating directional testis asymmetry to phenotypic quality. There were large differences between populations in testis size, with males from northern populations having larger testes than those from southern populations. Within populations, large testes were associated with larger body size and greater age. When the influence of these factors was removed statistically, males with large testes were more likely to be infected with haematozoan parasites, and had brighter yellow plumage. No evidence was found that directional asymmetry in testis size was related to either of these measures of phenotypic quality. These results are consistent with the hypothesis that males with large testes, while signalling higher phenotypic quality as revealed by increased plumage brightness, also pay a cost in terms of reduced immunocompetence, revealed by the increased probability of infection in these males. That these patterns were similar in three different populations adds further strength to these conclusions. Our results suggest that studying the sources of variation in testis size among individuals can reveal interesting processes in sexual selection.