The evolution of genital shape variation in female cetaceans*

Male genital diversification is likely the result of sexual selection. Female genital diversification may also result from sexual selection, although it is less well studied and understood. Female genitalia are complex among whales, dolphins, and porpoises, especially compared to other vertebrates. The evolutionary factors affecting the diversity of vaginal complexity could include ontogeny, allometry, phylogeny, sexual selection, and natural selection. We quantified shape variation in female genitalia using 2D geometric morphometric analysis, and validated the application of this method to study soft tissues. We explored patterns of variation in the shape of the cervix and vagina of 24 cetacean species (n = 61 specimens), and found that genital shape varies primarily in the relative vaginal length and overall aspect ratio of the reproductive tract. Extensive genital shape variation was partly explained by ontogenetic changes and evolutionary allometry among sexually mature cetaceans, whereas phylogenetic signal, relative testis size, and neonate size were not significantly associated with genital shape. Female genital shape is diverse and evolves rapidly even among closely related species, consistent with predictions of sexual selection models and with findings in invertebrate and vertebrate taxa. Future research exploring genital shape variation in 3D will offer new insights into evolutionary mechanisms because internal vaginal structures are variable and can form complex spirals.     

The mating systems of pinnipeds and marine iguanas: convergent evolution of polygyny

The convergent polygynous mating systems of marine iguanas and otariid pinnipeds depend on the existence of large female aggregations. These can build up where abundant marine food resources occur around oceanic islands which harbour fewer predators than continental areas. For marine iguanas distribution of food resources appears to determine the location of colonies, while for pinnipeds habitat choice is more decisive. In marine iguanas females benefit from gregariousness through reduced predation risk and social thermoregulation. In pinnipeds, sea lions may derive thermoregulatory benefits from gregariousness, while fur seals appear to be largely non-gregarious. In both groups males defend territories in areas of high female density. Large sexual size dimorphism presumably evolved in response to strong selection for high fighting potential of males. The capability to fast for prolonged periods of territory tenure is considered a secondary benefit of large male size, but not the driving force behind its evolution. We hypothesize that marginal males, through continuous sexual harassment of females that stay outside territories, have exerted pressure towards the evolution of female gregariousness.     

Sexual selection and the evolution of genital shape and complexity in water striders

Animal genitalia show two striking but incompletely understood evolutionary trends: a great evolutionary divergence in the shape of genitalic structures, and characteristic structural complexity. Both features are thought to result from sexual selection, but explicit comparative tests are hampered by the fact that it is difficult to quantify both morphological complexity and divergence in shape. We undertake a comparative study of multiple nongenitalic and male genital traits in a clade of 15 water strider species to quantify complexity and shape divergence. We show that genital structures are more complex and their shape more divergent among species than nongenital traits. Further, intromittent genital traits are more complex and have evolved more divergently than nonintromittent genital traits. More importantly, shape and complexity of nonintromittent genital traits show correlated evolution with indices of premating sexual selection and intromittent genital traits with postmating sexual selection, suggesting that the evolution of different components of genital morphology are shaped independently by distinct forms of sexual selection. Our quantitative results provide direct comparative support for the hypothesis that sexual selection is associated with morphological complexity in genitalic traits and highlight the importance of quantifying morphological shape and complexity, rather than size in studies of genital evolution.     

The coevolution of male and female genitalia in a mammal: A quantitative genetic insight

Male genitalia are among the most phenotypically diverse morphological traits, and sexual selection is widely accepted as being responsible for their evolutionary divergence. Studies of house mice suggest that the shape of the baculum (penis bone) affects male reproductive fitness and experimentally imposed postmating sexual selection has been shown to drive divergence in baculum shape across generations. Much less is known of the morphology of female genitalia and its coevolution with male genitalia. In light of this, we used a paternal half-sibling design to explore patterns of additive genetic variation and covariation underlying baculum shape and female vaginal tract size in house mice (Mus musculus domesticus). We applied a landmark-based morphometrics approach to measure baculum size and shape in males and the length of the vaginal tract and width of the cervix in females. Our results reveal significant additive genetic variation in house mouse baculum morphology and cervix width, as well as evidence for genetic covariation between male and female genital measures. Our data thereby provide novel insight into the potential for the coevolutionary divergence of male and female genital traits in a mammal.     

Sexual selection uncouples the evolution of brain and body size in pinnipeds

The size of the vertebrate brain is shaped by a variety of selective forces. Although larger brains (correcting for body size) are thought to confer fitness advantages, energetic limitations of this costly organ may lead to trade-offs, for example as recently suggested between sexual traits and neural tissue. Here, we examine the patterns of selection on male and female brain size in pinnipeds, a group where the strength of sexual selection differs markedly among species and between the sexes. Relative brain size was negatively associated with the intensity of sexual selection in males but not females. However, analyses of the rates of body and brain size evolution showed that this apparent trade-off between sexual selection and brain mass is driven by selection for increasing body mass rather than by an actual reduction in male brain size. Our results suggest that sexual selection has important effects on the allometric relationships of neural development.     

海洋哺乳动物信息素嗅觉的分子进化

研究感觉基因的进化规律是动物进化领域长期探索的重要问题.哺乳动物通常具有2套嗅觉系统:主要嗅觉系统(MOS)和犁鼻器系统(VNS).其中,VNS主要感知动物个体释放的信息素分子,而信息素在动物的生殖和社会行为中起重要调节作用.为了研究动物信息素嗅觉进化的背后推动力,对海洋哺乳动物的代表物种进行了Trpc2基因(VNS功能的分子标记)的序列测定和进化分析.以前的研究表明,Trpc2基因仅在VNS中表达,其序列完整/缺失与VNS的功能完整/退化完全一致.本研究结果显示,鲸类和海牛类的Trpc2为假基因,鳍脚类的1个分支类群(海豹类)和水獭类的Trpc2也是假基因,提示VNS功能丢失,即信息素嗅觉功能退化;而北极熊和鳍脚类的另一个分支类群(海狮类)保留了1个完整的Trpc2,并且这个基因仍受强烈的净化选择和功能限制,提示信息素嗅觉功能仍然保留.进一步分析表明,信息素嗅觉退化的海兽主要在水中交配,而信息素嗅觉保留的海兽主要在陆地上交配.本研究提出了一个新的科学假说:交配场所的选择可能推动了海洋哺乳动物信息素嗅觉的进化.     

MALE CONTEST COMPETITION AND THE COEVOLUTION OF WEAPONRY AND TESTES IN PINNIPEDS

Male reproductive success is influenced by competitive interactions during precopulatory and postcopulatory selective episodes. Consequently, males can gain reproductive advantages during precopulatory contest competition by investing in weaponry and during postcopulatory sperm competition by investing in ejaculates. However, recent theory predicts male expenditure on weaponry and ejaculates should be subject to a trade‐off, and should vary under increasing risk and intensity of sperm competition. Here, we provide the first comparative analysis of the prediction that expenditure on weaponry should be negatively associated with expenditure on testes mass. Specifically, we assess how sexual selection influences the evolution of primary and secondary sexual traits among pinnipeds (seals, sea lions, and walruses). Using recently developed comparative methods, we demonstrate that sexual selection promotes rapid divergence in body mass, sexual size dimorphism (SSD), and genital morphology. We then show that genital length appears to be positively associated with the strength of postcopulatory sexual selection. However, subsequent analyses reveal that both genital length and testes mass are negatively associated with investment in precopulatory weaponry. Thus, our results are congruent with recent theoretical predictions of contest‐based sperm competition models. We discuss the possible role of trade‐offs and allometry in influencing patterns of reproductive trait evolution in pinnipeds.     

Fractal analysis provides new insights into the complexity of marine mammal behavior: A review,two methods,their application to diving and surfacing patterns,and their relevance to marine mammal welfare assessment

Fractals have been applied to describe the complexity of behavioral displays in a range of organisms. Recent work suggests that they may represent a promising tool in the quantification of subtle behavioral responses in marine mammals under chronic exposure to disturbance. This paper aims at introducing the still seldom used fractals to the broader community of marine mammal scientists. We first briefly rehearse some of the fundamental principles behind fractal theory and review the previous uses of fractals in marine mammal science. We subsequently introduce two methods that may be used to assess the complexity of marine mammal diving patterns, and we apply them to the temporal dynamics of the diving patterns of killer whales in the presence and absence of sea kayaks, the sequential behavior of harbor and gray seals in environments with distinct levels of anthropogenic influence, and southern right whales with and without calves. We discuss the ecological relevance of identifying fractal properties in marine mammal behavior, and the potential strength of the fractal behavioral parameters in comparison to more standard behavioral metrics. We finally briefly address the relevance fractal methods may have for the design and implementation of management and conservation strategies.     

Sexual dimorphism in the baboon facial skeleton

Baboons exhibit marked sexual dimorphism in many aspects of their morphology. Dimorphism is especially pronounced in the face. We use finite-element analysis to investigate the ontogeny of sexual dimorphism in a cross-sectional sample of baboon (Papio sp.) faces. This method provides detailed quantitative information about size and shape changes at anatomical landmarks in the face during growth. Allometric results suggest that sexual dimorphism in facial size and shape is produced by ontogenetic scaling: males and females share a common ontogenetic trajectory. Analyses of growth in time, which complement allometric analyses, show that female growth slows much earlier than male growth, accounting for the differences between sexes. Local size and local shape follow similar patterns of growth, but changes in these variables are slower in females. Local and global facial size are much more dimorphic than local and global facial shape.     

Assessing the patterns and drivers of shape complexity in the amblypygid pedipalp

Amblypygi is an arachnid order possessing a unique pair of spined pedipalps: appendages that perform in prey capture, courtship, and contest. Pedipalp length, hypothesized to be under sexual selection, varies markedly across amblypygid species, and pedipalp spination, thought to reflect selection for function in prey capture, also differs interspecifically. Differences in pedipalp shape between species may indicate that the relative strength of selection for prey capture and sexual selection vary across the group. However, interspecific differences in pedipalp shape have not been quantified, due to difficulties in identifying homologous features. For the first time, we quantify trends in amblypygid pedipalp shape complexity. We use elliptical Fourier analysis to quantify 2D complexity in pedipalp outlines across eleven species and six genera. We find that complexity significantly decreases as pedipalp length increases. This appears to be driven by relative spine length, suggesting that a trade‐off exists between pedipalp length and spination. Furthermore, significant female‐biased sexual dimorphism in shape complexity is present in the tibial segment of the amblypygid pedipalp. Our results provide novel insights into the drivers of amblypygid pedipalp evolution and suggest that a functional trade‐off between performance in prey capture and other functions under sexual selection exist in this enigmatic structure.     

Cope's rule and the evolution of body size in Pinnipedimorpha (Mammalia: Carnivora)

Cope's rule describes the evolutionary trend for animal lineages to increase in body size over time. In this study, we tested the validity of Cope's rule for a marine mammal clade, the Pinnipedimorpha, which includes the extinct Desmatophocidae, and extant Phocidae (earless seals), Otariidae (fur seals and sea lions), and Odobenidae (walruses). We tested for the presence of Cope's rule by compiling a large dataset of body size data for extant and fossil pinnipeds and then examined how body size evolved through time. We found that there was a positive relationship between geologic age and body size. However, this trend is the result of differences between early assemblages of small-bodied pinnipeds (Oligocene to early Miocene) and later assemblages (middle Miocene to Pliocene) for which species exhibited greater size diversity. No significant differences were found between the number of increases or decreases in body size within Pinnipedimorpha or within specific pinniped clades. This suggests that the pinniped body size increase was driven by passive diversification into vacant niche space, with the common ancestor of Pinnipedimorpha occurring near the minimum adult body size possible for a marine mammal. Based upon the above results, the evolutionary history of pinnipeds does not follow Cope's rule.     

The evolution of male infanticide in relation to sexual selection in mammalian carnivores

The evolution of infanticide by males has often been explained by the sexual selection hypothesis, which posits that infanticide improves male reproductive success by shortening the interbirth intervals of the mothers of the killed offspring. In Carnivora, however, the fitness advantages assumed in this hypothesis have been shown in only a few species, and it has been argued that male infanticide may be nonadaptive in pinniped carnivores. According to the sexual selection hypothesis, male infanticide is expected to be more prevalent in species in which males are subjected to stronger sexual selection through intrasexual competition over mates. We examined a phylogenetically corrected relationship between male infanticide and sexual size dimorphism (SSD) as a measure of the intensity of sexual selection in carnivores. Our analyses failed to detect a significant association between the occurrence of male infanticide and SSD across carnivores, although they showed that, among fissipeds (typically terrestrial carnivores), males in species with stronger male-biased SSD are significantly more likely to commit infanticide. This suggests that the evolution of male infanticide is correlated with intense sexual selection in fissipeds. In pinnipeds (Odobenidae, Otariidae, and Phocidae), there was no significant association between male infanticide and SSD. Assuming that SSD represents the intensity of sexual selection on males, this result is consistent with the argument that infanticide by male pinnipeds is not a sexually selected behaviour.     

Social olfaction in marine mammals: wild female Australian sea lions can identify their pup's scent

Historically, anatomical evidence has suggested that marine mammals are anosmic or at best microsmatic, i.e. absent or reduced olfactory capabilities. However, these neuroanatomical considerations may not be appropriate predictors for the use of olfaction in social interactions. Observations suggest that pinnipeds may use olfaction in mother–pup interactions, accepting or rejecting pups after naso-nasal contact. Such maternal–offspring recognition is a favourable area for investigating the involvement of odours in social recognition and selectivity, as females are evolutionarily constrained to direct resources to filial young. However, there is no experimental, morphological or chemical evidence to date for the use of olfaction in social contexts and for individual odour recognition abilities in pinnipeds. Here, we report unequivocal evidence that Australian sea lion (Neophoca cinerea) females can differentiate between the odour of their own pup and that of another, in the absence of any other distinguishing cues. This study demonstrates individual olfactory recognition in a free-ranging wild mammal and is clear evidence of the social function of olfaction in a marine mammal.     

Morpho morphometrics: Shared ancestry and selection drive the evolution of wing size and shape in Morpho butterflies

Butterfly wings harbor highly diverse phenotypes and are involved in many functions. Wing size and shape result from interactions between adaptive processes, phylogenetic history, and developmental constraints, which are complex to disentangle. Here, we focus on the genus Morpho (Nymphalidae: Satyrinae, 30 species), which presents a high diversity of sizes, shapes, and color patterns. First, we generate a comprehensive molecular phylogeny of these 30 species. Next, using 911 collection specimens, we quantify the variation of wing size and shape across species, to assess the importance of shared ancestry, microhabitat use, and sexual selection in the evolution of the wings. While accounting for phylogenetic and allometric effects, we detect a significant difference in wing shape but not size among microhabitats. Fore and hindwings covary at the individual and species levels, and the covariation differs among microhabitats. However, the microhabitat structure in covariation disappears when phylogenetic relationships are taken into account. Our results demonstrate that microhabitat has driven wing shape evolution, although it has not strongly affected forewing and hindwing integration. We also found that sexual dimorphism of forewing shape and color pattern are coupled, suggesting a common selective force.     

Systematics, biostratigraphy and evolutionary pattern of the Oligo-Miocene marine mammals from the Maltese Islands

An overview of the upper Oligocene-upper Miocene marine sediments outcropping in the Maltese Islands provides a detailed stratigraphical setting of several marine mammal assemblages. The studied fossil material collected within the entire sequence, is now kept in the National Museum of Natural History of Mdina (Malta). Nannoplankton analysis of some selected sections, where mammal remains have been discovered, is also undertaken. The fossil marine mammals, consisting mostly of isolated ear bones and teeth, are referred to cetaceans (both mysticetes and odontocetes), sirenians, and pinnipeds. The cetacean record evidences an evolutionary pattern that agrees with the Oligo-Miocene general trend, characterized by the progressive rarefaction and disappearance of archaic families (squalodontids, waipatiids, and, maybe, mammalodontids), and by the appearance and diversification of the extant families represented within younger strata (kogiids, pontoporiids and ziphiids). Pontoporiids, waipatiids, and tentatively mammalodontids are here reported for the first time in the Mediterranean, while the kogiid record represents the only sure Miocene evidence of this family in the Mediterranean. The geographical distribution of the mammalodontids and the waipatiids, based on the Maltese and extra-Mediterranean records, supports an open communication between the Proto-Mediterranean and the Indo-Pacific during the late Oligocene. Sirenians are represented by several dugongid pachyosteosclerotic rib fragments, collected from upper Oligocene through upper Miocene sediments. Pinnipeds are represented by a femur fragment from the Serravallian, referred to an indeterminate monachine, a phocid subfamily already reported from the Mio-Pliocene of the Mediterranean.     

SEXUAL SELECTION AND THE EVOLUTION OF COMPLEX COLOR PATTERNS IN DRAGON LIZARDS

Many species have elaborate and complex coloration and patterning, which often differ between the sexes. Sexual selection may increase the size or intensity of color patches (elaboration) in one sex or drive the evolution of novel signal elements (innovation). The latter potentially increases color pattern complexity. Color pattern complexity may also be influenced by ecological factors related to predation and environment; however, very few studies have investigated the effects of both sexual and natural selection on color pattern complexity across species. We used a phylogenetic comparative approach to examine these effects in 85 species and subspecies of Australian dragon lizards (family Agamidae). We quantified color pattern complexity by adapting the Shannon–Wiener diversity index. There were clear sex differences in color pattern complexity, which were positively correlated with both sexual dichromatism and sexual size dimorphism, consistent with the idea that sexual selection plays a significant role in the evolution of color pattern complexity. By contrast, we found little evidence of a link between environmental factors and color pattern complexity on body regions exposed to predators. Our results suggest that sexual selection rather than natural selection has led to increased color pattern complexity in males.     

Is sexual selection driving diversification of the bioluminescent ponyfishes (Teleostei: Leiognathidae)?

Sexual selection may facilitate genetic isolation among populations and result in increased rates of diversification. As a mechanism driving diversification, sexual selection has been invoked and upheld in numerous empirical studies across disparate taxa, including birds, plants and spiders. In this study, we investigate the potential impact of sexual selection on the tempo and mode of ponyfish evolution. Ponyfishes (Leiognathidae) are bioluminescent marine fishes that exhibit sexually dimorphic features of their unique light-organ system (LOS). Although sexual selection is widely considered to be the driving force behind ponyfish speciation, this hypothesis has never been formally tested. Given that some leiognathid species have a sexually dimorphic LOS, whereas others do not, this family provides an excellent system within which to study the potential role of sexual selection in diversification and morphological differentiation. In this study, we estimate the phylogenetic relationships and divergence times for Leiognathidae, investigate the tempo and mode of ponyfish diversification, and explore morphological shape disparity among leiognathid clades. We recover strong support for a monophyletic Leiognathidae and estimate that all major ponyfish lineages evolved during the Paleogene. Our studies of ponyfish diversification demonstrate that there is no conclusive evidence that sexually dimorphic clades are significantly more species rich than nonsexually dimorphic lineages and that evidence is lacking to support any significant diversification rate increases within ponyfishes. Further, we detected a lineage-through-time signal indicating that ponyfishes have continuously diversified through time, which is in contrast to many recent diversification studies that identify lineage-through-time patterns that support mechanisms of density-dependent speciation. Additionally, there is no evidence of sexual selection hindering morphological diversity, as sexually dimorphic taxa are shown to be more disparate in overall shape morphology than nonsexually dimorphic taxa. Our results suggest that if sexual selection is occurring in ponyfish evolution, it is likely acting only as a genetic isolating mechanism that has allowed ponyfishes to continuously diversify over time, with no overall impact on increases in diversification rate or morphological disparity.     

Recovery Trends in Marine Mammal Populations

Marine mammals have greatly benefitted from a shift from resource exploitation towards conservation. Often lauded as symbols of conservation success, some marine mammal populations have shown remarkable recoveries after severe depletions. Others have remained at low abundance levels, continued to decline, or become extinct or extirpated. Here we provide a quantitative assessment of (1) publicly available population-level abundance data for marine mammals worldwide, (2) abundance trends and recovery status, and (3) historic population decline and recent recovery. We compiled 182 population abundance time series for 47 species and identified major data gaps. In order to compare across the largest possible set of time series with varying data quality, quantity and frequency, we considered an increase in population abundance as evidence of recovery. Using robust log-linear regression over three generations, we were able to classify abundance trends for 92 spatially non-overlapping populations as Significantly Increasing (42%), Significantly Decreasing (10%), Non-Significant Change (28%) and Unknown (20%). Our results were comparable to IUCN classifications for equivalent species. Among different groupings, pinnipeds and other marine mammals (sirenians, polar bears and otters) showed the highest proportion of recovering populations, likely benefiting from relatively fast life histories and nearshore habitats that provided visibility and protective management measures. Recovery was less frequent among cetaceans, but more common in coastal than offshore populations. For marine mammals with available historical abundance estimates (n = 47), larger historical population declines were associated with low or variable recent recoveries so far. Overall, our results show that many formerly depleted marine mammal populations are recovering. However, data-deficient populations and those with decreasing and non-significant trends require attention. In particular, increased study of populations with major data gaps, including offshore small cetaceans, cryptic species, and marine mammals in low latitudes and developing nations, is needed to better understand the status of marine mammal populations worldwide.