Zur Ursache des Hodenabstiegs (Descensus testiculorum) bei Säugetieren1

On the cause of the mammalian descent of the testes (Descensus testiculorum) Two explanations have been offered for the descent of the testes in mammals, both of which are frequently cited in the literature. Moore and co-workers argued that the phylogenetic rise of body temperature caused the translocation of the testes. According to Portmann , the descent of the testes was due to the evolution of the scrotum as a signal. However, both the sensibility of the extra-abdominal testes to temperature elevations and the optical effects of the scrotum can be interpreted as a consequence of testicular descent rather than as its cause. The hypothesis presented in this paper suggests a new adaptive explanation for the descent of the testes in mammals and regards its development as an example of evolutionary compromise. Obvious disadvantages such as reduced protection of the extra-abdominal testes, “perforation” of the inguinal abdominal wall, and an increased loss of heat from the body core have to be outbalanced by a strong selective advantage. This advantage is seen in the development of a completely new, fast mode of locomotion - the gallop. The strong flexions and extensions of the vertebral column during gallop should cause intense fluctuations of intra-abdominal pressure. Fluctuations of intra-abdominal pressure severely impede continuous flow of blood in the abdominal veins. Periodically reduced venous drainage resulting in fluctuations of intra-testicular pressure would impair the process of spermiohistogenesis, which is dependent on an absolutely constant pressure within the testis. Thus, it is the displacement of the pressure sensitive testes out of the abdominal cavity that allows for the evolution of a fast mode of locomotion accompanied by strong fluctuations of intraabdominal pressure. In the course of the phylogenetic translocation of the testes increasing specializations of the testicular blood vessels occur. In mammals possessing a scrotum the return flow of venous blood from the extra-abdominal testes to the abdominal cavity is supported by utilizing the energy of the arterial pulse (‘peripheral arterial pump’). A model for the successive stages of the descent of the testes is illustrated in Figures 7–10. The morphological changes related to the phylogenetic descent of the testes, such as the specialization of the testicular blood vessels, the forming of a cremasteric sack in the inguinal region, and the differentiation of the inguinal or perineal integument into a scrotum can all be interpreted as serving one purpose: they aid in maintaining a constant intra-testicular pressure in spite of increasing fluctuations of intra-abdominal pressure and venous blood flow during the evolution of the gallop. Although the blood vessels of the spermatic chord basically serve the same functions, they show markedly different specializations in Marsupials and Eutherians. This indicates that the descent of the testes has occurred independently, at least, in these two groups. The explanation put forward here postulates a causal relationship between the mode of locomotion and the position of the testes. Mammals possessing testes wnich reside permanently within the abdominal cavity (‘Testiconda’) cannot gallop, whereas mammals with the ability to gallop must have (periodical or permanent) extraabdominal testes (‘Testiphaena’).     

Sweat glands of the scrotum of the bull

Skin samples were taken post mortem from the scrotum, abdomen and neck of 4 mature bulls. The volume of sweat glands per unit skin surface area of the scrotum was greater than that of other body regions. Within the scrotum there was a gradient in sweat gland volume increasing from proximal through to distal parts of the scrotum. These results suggest a previously unidentified variable cooling capacity of the scrotum depending on testicular descent.     

Dental eruption in afrotherian mammals

Background  

Afrotheria comprises a newly recognized clade of mammals with strong molecular evidence for its monophyly. In contrast, morphological data uniting its diverse constituents, including elephants, sea cows, hyraxes, aardvarks, sengis, tenrecs and golden moles, have been difficult to identify. Here, we suggest relatively late eruption of the permanent dentition as a shared characteristic of afrotherian mammals. This characteristic and other features (such as vertebral anomalies and testicondy) recall the phenotype of a human genetic pathology (cleidocranial dysplasia), correlations with which have not been explored previously in the context of character evolution within the recently established phylogeny of living mammalian clades.     

A transgenic insertion causing cryptorchidism in mice

A distinctive feature of gonadal maturation in mammals is the movement to an extraabdominal location. Testicular descent is a complex, multistage process whereby the embryonic gonads migrate from their initial abdominal position to the scrotum. Failure in this process results in cryptorchidism, a frequent congenital birth defect in humans. We report here a new mouse transgenic insertional mutation, cryptorchidism with white spotting (crsp). Males homozygous for crsp exhibit a high intraabdominal position of the testes, associated with complete sterility. Heterozygous males have a wild-type phenotype, and homozygous females are fertile. Surgically descended testes in crsp/crsp males show normal spermatogenesis. Using FISH and genetic analyses, the transgenic insert causing the crsp mutation has been mapped to the distal part of mouse chromosome 5. Transgene integration resulted in a 550-kb deletion located upstream of the Brca2 gene. A candidate gene encoding a novel G protein-coupled receptor (Great) with an expression pattern suggesting involvement in testicular descent has been identified.     

Age-Related and Individual Anatomical Variation in Testicular Topography in Human Fetuses

At present, male infertility remains an urgent medical concern. From year to year, despite advances in methods of diagnosis and treatment, medicine encounters an increasing number of infertile couples with male infertility playing a leading role. Prerequisites for fertility disorders very frequently appear in childhood. Urologists consider cryptorchidism a leading cause of male infertility. The aim of our study was to establish the relationship between testicular descent to the scrotum and the age of the fetus. Material and methods. The study was conducted using 195 specimens of male fetuses aged 4–10 months with 81.0–375.0 mm parietalcoccygeal length (PCL) using the methods of macromicroscopic, conventional, and microslide preparation under control of binocular loupes and morphometry. Results. At the beginning of the fetal period of human ontogenesis (fetuses 81.0–135.0 mm PCL), the right and left testicles are mainly located above the corresponding deep inguinal ring and they are less often located in a region of the iliac fossae. An analysis of topographic and anatomical features of the male reproductive glands in 5-month-old fetuses (136.0–185.0 mm PCL) revealed that the testicles were located within the large pelvis, with the lower end of both the right and left testicles located above the entrance to the deep inguinal ring at a distance that equals the length of the pelvic part of the gubernaculum testis—3.2 ± 0.3 mm (right) and 2.8 ± 0.2 mm (left). In 11 fetuses aged 7 months (231.0–270.0 mm PCL), the lower ends of the testicles and their gubernaculum testis are immersed in the corresponding deep inguinal ring. In eight fetuses, the testicles were within the deep inguinal ring. A combination of many factors contributes to the final migration of a testicle through the inguinal canal into the scrotum (fetuses: 270.0 cm–290.0 mm PCL), including muscle contraction of the anterolateral abdominal wall, an increase in intra-abdominal pressure, contractile capacity of the gubernaculum testis of the testicle, the vaginal process of the peritoneum, and the neuro-muscular system. We believe that the gubernaculum testis is a particularly significant factor in testicular descent to the scrotum. The gubernaculum testis is maximally developed prior to migration of a testicle through the inguinal canal (eighth month of antenatal development), as evidenced by the prevalence of smooth muscle cells over connective tissue elements. An analysis of testicular topography in fetuses aged 9 months (311.0–345.0 mm PCL) revealed that testicles were located in the scrotum in nine fetuses, near the superficial inguinal ring in six fetuses, within the inguinal canal in four cases, and in the deep inguinal ring in one case. In fetuses aged 10 months (346.0–375.0 mm PCL), testicles were located in the scrotum in 13 cases and within the inguinal canal in seven cases. According to our research, the fusion of layers of the vaginal process of the peritoneum occurs in fetuses aged 9–10 months, resulting in the disappearance of the communication of its cavity with the peritoneum. A delay in the fusion of the peritoneal vaginal process layers at the end of the fetal period is an anatomic prerequisite for the occurrence of congenital inguinal-scrotal hernias. Conclusions. It has been found that the rate of testicular descent to the scrotum does not always coincide with the corresponding stage of fetal development. An accelerated development of the gubernaculum testis in fetuses aged 5–8 months is a major factor of heterochronic development of a testicle and subsequent testicular descent into the scrotum.     

Müllerian inhibiting substance production and testicular migration and descent in the pouch young of a marsupial

The ontogeny of Müllerian inhibiting substance (MIS) production by the developing testis of an Australian marsupial, the tammar wallaby (Macropus eugenii), was determined during pouch life using an organ-culture bioassay of mouse fetal urogenital ridge. This information was related to the morphological events during testicular migration and descent. MIS biological activity was found in testes (but not ovaries or liver) of pouch young from 2 to 85 days of age. MIS production had commenced by day 2, which is within a day of the first gross morphological signs of testicular differentiation. Müllerian duct regression occurred between 10 and 30 days, which partly coincided with testicular migration to the inguinal region and enlargement of the gubernacular bulb (15 to 30 days). These observations are consistent with the hypothesis that MIS may be involved in testicular transabdominal migration. The epididymis commenced development and growth only after the testis had descended through the inguinal ring. This provides no support for the suggestion that the epididymis is involved in testicular descent into the scrotum. The basic sequence of events in post-testicular sexual differentiation in the wallaby is sufficiently similar to that seen in eutherian mammals to make it an excellent experimental model for future studies of testicular differentiation, migration and descent.     

The obligately lichenicolous genus Lichenoconium represents a novel lineage in the Dothideomycetes

Lichenicolous fungi are obligately lichen-associated organisms that have evolved many times throughout the Ascomycota and Basidiomycota. Approximately 20% of lichenicolous ascomycetes are recognized only from asexual (anamorphic) characteristics, so the phylogenetic position of many groups has never been resolved. Here we present the first molecular phylogeny of Lichenoconium, a genus of strictly asexual, obligately lichenicolous species with broad geographic distributions and diverse host ecologies. We obtained nuclear and mitochondrial rDNA sequences from fungal cultures isolated from four species in the genus, including a new species, Lichenoconium aeruginosum sp. nov., collected in France, Luxembourg and Netherlands. Our multilocus phylogeny supports the monophyly of fungi in the genus Lichenoconium, and places the genus in the Dothideomycetes, an ascomycete class made up mainly of saprobes and plant-associated endophytes and pathogens. There are only a few recognized groups of lichen-formers in the Dothideomycetes, but Lichenoconium is not supported as being closely related to any of these, nor to any other recognized order within the Dothideomycetes. Given that Lichenoconium is but one of over 100 genera of anamorphic lichenicolous fungi, most of which have never been studied phylogenetically, we suggest that asexual lichenicolous fungi may represent novel and evolutionarily significant phylogenetic groups in the Kingdom Fungi.     

New Studies of Enamel Microstructure in Mesozoic Mammals: A Review of Enamel Prisms as a Mammalian Synapomorphy

Characters from enamel microstructure have not been used in recent phylogenetic analyses of Mesozoic Mammalia. Reasons are that enamel characters have been perceived as (A) variable without regard to systematic position of taxa, (B) inconsistently reported within the literature, and (C) simply scored as either prismatic or not prismatic in earlier mammals. Our work on Mesozoic mammals such as Sinoconodon, Gobiconodon, Triconodontidae, Docodon, Laolestes, and others suggests that synapsid columnar enamel (SCE) structure was easily transformed into plesiomorphic prismatic enamel (PPE) and that PPE may be described with at least five independent character states. Two PPE characters—a flat, open prism sheath and a planar prism seam—were present in the cynodont Pachygenelus and in several Jurassic and Cretaceous mammals. We propose that appearance of a prism sheath transforms SCE into PPE and that reduction and loss of a prism sheath reverse PPE into SCE, in both phylogeny and ontogeny. We further propose that no amniote vertebrates other than the trithelodontid cynodont, Pachygenelus, plus Mammalia have ever evolved an ameloblastic Tomes process capable of secreting PPE and that the genetic potential to secrete PPE is a synapomorphy of Pachygenelus plus Mammalia, whether or not all lineages of the clade have expressed that potential.     

Rapid diversification, incomplete isolation, and the "speciation clock" in North American salamanders (Genus Plethodon): testing the hybrid swarm hypothesis of rapid radiation

The history of life has been marked by several spectacular radiations, in which many lineages arise over a short period of time. A possible consequence of such rapid splitting in the recent past is that the intrinsic barriers that prevent gene flow between many species may have too little time to develop fully, leading to extensive hybridization among recently evolved lineages. The salamander genus Plethodon in eastern North America has been proposed as a possible example of this scenario, but without explicit statistical tests. In this paper, we present a nearly comprehensive phylogeny for the 45 extant species of eastern Plethodon, based on DNA sequences of mitochondrial (two genes, 1335 base pairs) and nuclear genes (two genes, up to 3481 base pairs). We then use this phylogeny to examine rates and patterns of diversification and hybridization. We find significantly rapid diversification within the glutinosus species group. Examining patterns of natural hybridization in light of the phylogeny shows considerable hybridization within this clade, including introgression between species that are morphologically distinct and distantly related. Reproductive isolation increases over time and may be very weak among the most recently diverged species. These results suggest that the origin of species and the evolution of intrinsic reproductive isolating mechanisms, rather than being synonymous, may be decoupled in some cases (i.e., rapid origin of lineages outstrips the "speciation clock"). In contrast to the conclusions of a recent review of adaptive radiation and hybridization, we suggest that extensive hybridization sometimes may be a consequence, rather than a cause, of rapid diversification.     

Anomalies de position des testicules dans l’enfance: conséquences à l’âge adulte

Non descended testes in the low scrotum is a common anomaly at birth, with about 4% of the newborn males affected. Only one quarter of these newborn babies will still have non descended testes when one year old. However, the testes that will descend within the first year of life seem no more to be considered as normally descended testes. Moreover, the retractile testis, which represents a secondary anomaly of testicular position occuring after the babies are older than one year, is no more to be regarded as a physiological variant of the normally descended testis, since several reports indicate histological and clinical modifications in such cases. The testicular non descent can be associated with two consequences in adult life. Firstly, an history of non descended testis is the only known risk factor for the testicular cancer. Secondly, such an history is a risk factor for the male fertility because of spermatogenesis alterations, as indicated by qualitative and quantitative histological analyses of the testicular tissue, and by depressed spermatozoa output and quality (motility, normal forms); moreover, testicular volumes are reduced, and the time to pregnancy as well as the rate of infertility are increased. Time is arrived for a reappraisal of the consequences in adult life of the abnormal testicular location (either congenital or acquired) during childhood.     

The evolution of the scrotum: a new hypothesis

The adaptive significance of the scrotum is unresolved after more than 60 years of debate and experimentation. The "training hypothesis" introduced here suggests that testicular descent is a mechanism for improving sperm quality. The hypothesis proposes that: (1) testicular descent decreases blood supply to maturing sperm cells, (2) sperm mitochondria respond to the resulting oxygen stress by enhancing their enzymatic machinery for oxidative metabolism, as do oxygen-stressed muscle cell mitochondria, and (3) the resulting increase in aerobic fitness of sperm cells is advantageous in inter-ejaculate competition. The hypothesis suggests that there is a quantity-quality trade-off in sperm production, where taxa with internal testes produce large volumes of low-quality sperm while taxa with scrotal testes produce smaller volumes of higher-quality sperm.     

Re‐evaluating the distribution of cooperative breeding in birds: is it tightly linked with altriciality?

The evolution of cooperative breeding (CB) in birds has aroused intensive interest for decades, largely due to the paradox that some adults forgo independent breeding to help others. While much effort has been directed at understanding the adaptive significance of CB behavior, much less effort has been spent on understanding its origin. Ligon and Burt argued that the evolution of altriciality played a key role in the origin of CB since CB occurs more frequently in altricial lineages than expected if developmental mode and CB evolved independently and that both traits arose early in the avian tree of life. We mapped presence or absence of CB, and precocial or altricial development on a recent phylogeny of all birds to re‐evaluate their conclusions. Our results suggest altriciality may be more recently derived than previously thought, and that CB species clustered in a derived land bird clade (especially within Passeriformes) where we reconstructed many gains and losses. We did find a link between cooperative breeding and altriciality. However, since CB also occurs in precocial species, has not evolved in many altricial clades, and may have evolved prior to altriciality (based on some classifications of which species have CB), it is not clear whether altriciality is linked to other factors, such as benefits to group living, that are necessary for the acquisition of CB behavior, or whether altriciality may have been a driving force in the evolution of CB itself. The relative importance of these other factors versus altriciality for the origin of CB needs to be considered.     

Giardia: highly evolved parasite or early branching eukaryote?

The phylogeny of the commonest protozoal agent of intestinal disease, Giardia, is unclear. Although recent intensive research suggests this important human parasite is an early branching eukaryote that evolved before the endosymbiotic origin of mitochondria, there is also evidence to suggest that, as a highly evolved parasite, it has lost many of its ancestral characteristics. In this case, these organisms might have arisen much more recently from aerobic free-living flagellates.     

The descended larynx is not uniquely human

Morphological modifications of vocal anatomy are widespread among vertebrates, and the investigation of the physiological mechanisms and adaptive functions of such variants is an important focus of research into the evolution of communication. The "descended larynx" of adult humans has traditionally been considered unique to our species, representing an adaptation for articulate speech, and debate concerning the position of the larynx in extinct hominids assumes that a lowered larynx is diagnostic of speech and language. Here, we use bioacoustic analyses of vocalizing animals, together with anatomical analyses of functional morphology, to document descended larynges in red and fallow deer. The resting position of the larynx in males of these species is similar to that in humans, and, during roaring, red-deer stags lower the larynx even further, to the sternum. These findings indicate that laryngeal descent is not uniquely human and has evolved at least twice in independent lineages. We suggest that laryngeal descent serves to elongate the vocal tract, allowing callers to exaggerate their perceived body size by decreasing vocal-tract resonant frequencies. Vocal-tract elongation is common in birds and is probably present in additional mammals. Size exaggeration provides a non-linguistic alternative hypothesis for the descent of the larynx in human evolution.     

Sex determination in marsupials: evidence for a marsupial-eutherian dichotomy

In this paper, we review briefly the current state of knowledge about sexual differentiation in eutherian mammals, and then describe the situation in detail in two marsupial species: the North American opossum and the tammar wallaby. The conventional explanation for the genesis of all male somatic sexual dimorphisms in mammals is that they are a consequence of the systemic action of testicular hormones. In the absence of testes, the embryo will develop a female phenotype. We present evidence for the tammar wallaby that calls into question the universal applicability of this hormonal theory of mammalian sexual differentiation. We have shown that extensive somatic sexual dimorphisms precede by many days the first morphological evidence of testicular formation, which does not occur until around the third day of pouch life. Male foetuses, and pouch young on the day of birth, already have a well-developed gubernaculum and processus vaginalis, paired scrotal anlagen, and a complete absence of mammary anlagen, whereas female foetuses and newborn pouch young have a poorly developed gubernaculum and processus vaginalis, no scrotal anlagen, and well-developed mammary anlagen. Because it seems unlikely that the male gonad could begin hormone secretion until after the Sertoli and Leydig cells are developed, our results strongly suggest that some sexually dimorphic somatic characteristics develop autonomously, depending on their genotype rather than the hormonal environment to which they are exposed. We have been able to confirm the hormonal independence of the scrotum, pouch and mammary gland by administering testosterone propionate daily by mouth to female pouch young from the day of birth; although the Wolffian duct was hyperstimulated, there was no sign of scrotal development, or pouch or mammary inhibition. When male pouch young were treated with oestradiol benzoate in a similar fashion, there was hyperstimulation of the Müllerian duct and inhibition of testicular migration and development, but no sign of scrotal inhibition or pouch or mammary development. Our results in the tammar wallaby are consistent with the earlier studies on the opossum, whose significance was not appreciated at the time. Further evidence in support of this hormonal independence comes from earlier studies of spontaneously occurring intersexes in several species of marsupial, including the opossum and the tammar wallaby. An XXY individual had intra-abdominal testes and complete masculinization of the male reproductive tract internally, but externally there was a pouch and mammary glands and no scrotum.(ABSTRACT TRUNCATED AT 400 WORDS)     

Exploring the phylogenetic history of mammal species richness

Aim At broad geographical scales, species richness is a product of three basic processes: speciation, extinction and migration. However, determining which of these processes predominates is a major challenge. Whilst palaeontological studies can provide information on speciation and extinction rates, data are frequently lacking. Here we use a recent dated phylogenetic tree of mammals to explore the relative importance of these three processes in structuring present‐day richness gradients. Location The global terrestrial biosphere. Methods We combine macroecological data with phylogenetic methods more typically used in community ecology to describe the phylogenetic history of regional faunas. Using simulations, we explore two simple phylogenetic metrics, the mean and variance in the pairwise distances between taxa, and describe their relationship to phylogenetic tree topology. We then use these two metrics to characterize the evolutionary relationships among mammal species assemblages across the terrestrial biome. Results We show that the mean and variance in the pairwise distances describe phylogenetic tree topology well, but are less sensitive to phylogenetic uncertainty than more direct measures of tree shape. We find the phylogeny for South American mammals is imbalanced and ‘stemmy’ (long branches towards the root), consistent with recent diversification within evolutionarily disparate lineages. In contrast, the phylogeny for African mammals is balanced and ‘tippy’ (long branches towards the tips), more consistent with the slow accumulation of diversity over long times, reflecting the Old World origin of many mammal clades. Main conclusions We show that phylogeny can accurately capture biogeographical processes operating at broad spatial scales and over long time periods. Our results support inferences from the fossil record – that the New World tropics are a diversity cradle whereas the Old World tropics are a museum of old diversity.     

GREAT/LGR8 is the only receptor for insulin-like 3 peptide

During male development testes descend from their embryonic intraabdominal position into the scrotum. Two genes, encoding the insulin-like 3 peptide (INSL3) and the GREAT/LGR8 G protein-coupled receptor, control the differentiation of gubernaculum, the caudal genitoinguinal ligament critical for testicular descent. It was established that the INSL3 peptide activates GREAT/LGR8 receptor in vitro. Mutations of Insl3 or Great cause cryptorchidism (undescended testes) in mice. Overexpression of the transgenic Insl3 causes male-like gubernaculum differentiation, ovarian descent into lower abdominal position, and reduced fertility in females. To address the question whether Great deletion complements the mutant female phenotype caused by the Insl3 overexpression, we have produced Insl3 transgenic mice deficient for Great. Such females had a wild-type phenotype, demonstrating that Great was the only cognate receptor for Insl3 in vivo. We have established that pancreatic HIT cells, transfected with the INSL3 cDNA, produce functionally active peptide. Analysis of five INSL3 mutant variants detected in cryptorchid patients showed that P49S substitution renders functionally compromised peptide. Therefore, mutations in INSL3 might contribute to the etiology of cryptorchidism. We have also showed that synthetic insulin-like peptides (INSL4 and INSL6) were unable to activate LGR7 or GREAT/LGR8.     

Cryptorchidism in mice with an androgen receptor ablation in gubernaculum testis

Androgens play a critical role in the development of the male reproductive system, including the positioning of the gonads. It is not clear, however, which developmental processes are influenced by androgens and what are the target tissues and cells mediating androgen signaling during testicular descent. Using a Cre-loxP approach, we have produced male mice (GU-ARKO) with conditional inactivation of the androgen receptor (Ar) gene in the gubernacular ligament connecting the epididymis to the caudal abdominal wall. The GU-ARKO males had normal testosterone levels but developed cryptorchidism with the testes located in a suprascrotal position. Although initially subfertile, the GU-ARKO males became sterile with age. We have shown that during development, the mutant gubernaculum failed to undergo eversion, a process giving rise to the processus vaginalis, a peritoneal outpouching inside the scrotum. As a result, the cremasteric sac did not form properly, and the testes remained in the low abdominal position. Abnormal development of the cremaster muscles in the GU-ARKO males suggested the participation of androgens in myogenic differentiation; however, males with conditional AR inactivation in the striated or smooth muscle cells had a normal testicular descent. Gene expression analysis showed that AR deficiency in GU-ARKO males led to the misexpression of genes involved in muscle differentiation, cell signaling, and extracellular space remodeling. We therefore conclude that AR signaling in gubernacular cells is required for gubernaculum eversion and outgrowth. The GU-ARKO mice provide a valuable model of isolated cryptorchidism, one of the most common birth defects in newborn boys.