Phylogenetic analysis of viviparity, matrotrophy, and other reproductive patterns in chondrichthyan fishes.

The reproductive diversity of extant cartilaginous fishes (class Chondrichthyes) is extraordinarily broad, reflecting more than 400 million years of evolutionary history. Among their many notable reproductive specialisations are viviparity (live-bearing reproduction) and matrotrophy (maternal provision of nutrients during gestation). However, attempts to understand the evolution of these traits have yielded highly discrepant conclusions. Here, we compile and analyse the current knowledge on the evolution of reproductive diversity in Chondrichthyes with particular foci on the frequency, phylogenetic distribution, and directionality of evolutionary changes in their modes of reproduction. To characterise the evolutionary transformations, we amassed the largest empirical data set of reproductive parameters to date covering nearly 800 extant species and analysed it via a comprehensive molecular-based phylogeny. Our phylogenetic reconstructions indicated that the ancestral pattern for Chondrichthyes is 'short single oviparity' (as found in extant holocephalans) in which females lay successive clutches (broods) of one or two eggs. Viviparity has originated at least 12 times, with 10 origins among sharks, one in batoids, and (based on published evidence) another potential origin in a fossil holocephalan. Substantial matrotrophy has evolved at least six times, including one origin of placentotrophy, three separate origins of oophagy (egg ingestion), and two origins of histotrophy (uptake of uterine secretions). In two clades, placentation was replaced by histotrophy. Unlike past reconstructions, our analysis reveals no evidence that viviparity has ever reverted to oviparity in this group. Both viviparity and matrotrophy have arisen by a variety of evolutionary sequences. In addition, the ancestral pattern of oviparity has given rise to three distinct egg-laying patterns that increased clutch (brood) size and/or involved deposition of eggs at advanced stages of development. Geologically, the ancestral oviparous pattern arose in the Paleozoic. Most origins of viviparity and matrotrophy date to the Mesozoic, while a few that are represented at low taxonomic levels are of Cenozoic origin. Coupled with other recent work, this review points the way towards an emerging consensus on reproductive evolution in chondrichthyans while offering a basis for future functional and evolutionary analyses. This review also contributes to conservation efforts by highlighting taxa whose reproductive specialisations reflect distinctive evolutionary trajectories and that deserve special protection and further investigation.

Gene flow from rhesus (Macaca mulatta) to cynomolgus macaques (M. fascicularis) and effects of introgressive hybridization on reproduction in two biomedically relevant non-human primate species.

BACKGROUND: We compared the reproductive patterns of wild Indochinese and Sundaic cynomolgus macaques (Mf) exhibiting different levels of genetic admixture with rhesus macaques (Mm). METHODS: Ten adult females from each Indochinese (WHM) and Sundaic (KN/KTK) Mf populations, which exhibited 50% and 15% of Mm autosomal SNPs, were selected as focal animals. Animals were observed for 12 months, and the frequencies of sexual proceptivity, attractivity and receptivity, number of newborns, and changes in sex skin were recorded. RESULTS: Both populations showed all three sexual behaviors throughout the year, but they were classified as moderately seasonal breeders because their 3-month birth counts were as high as ~50%. The fecundity of WHM was lower than the KN/KTK. Changes in sex skin of WHM were more prone to Mm's pattern than the KN/KTK. CONCLUSION: The introgressive gene flow from Mm to Mf does not affect Mf's sexual behaviors; however, it can impact fecundity and physiological (sex skin) changes.

Evaluation of the reproductive profile of Subulina octona (Gastropoda, Subulinidae) experimentally infected by Paratanaisia bragai (Digenea, Eucotylidae) / Avaliação do perfil reprodutivo de Subulina octona (Gastropoda, Subulinidae) infectada experimentalmente por Paratanaisia bragai (Digenea, Eucotylidae)

Abstract Snails infected by trematodes may increase or decrease their reproductive activity in response to the presence of infection. Our aim was to verify the reproductive alterations in Subulina octona after infection by Paratanaisia bragai. The infected snails were individually exposed for 24 hours to 20 parasite eggs and four groups were formed (10, 20, 30 and 40 d.p.i.- days after infection), along with control groups. Every 10 days, the number of eggs in the reproductive tract, number of eggs hatched, galactogen content and histopathological changes were evaluated. The reproductive in the control and infected snails presented an alternating pattern, where periods of high production of eggs and newly hatched were followed by periods of low production. However, in relation to the amount of galactogen, both control and infected groups followed the same pattern of variation. In the histology, we observed the presence of male and female gametes with marked reduction in the number of oocytes. The results indicate that the intra-snail development of the parasite affects the reproductive biology of the host.

Resumo Moluscos infectados por trematódeos podem aumentar ou diminuir sua atividade reprodutiva em resposta à presença da infecção. Nosso objetivo foi verificar as alterações reprodutivas de Subulina octona após a infecção por Paratanaisia bragai. Os moluscos infectados foram individualmente expostos durante 24 horas a 20 ovos do parasito e quatro grupos foram formados (10, 20, 30 e 40 d.p.i. - dias pós infecção), com respectivos grupos controle. A cada 10 dias, o número de ovos no trato reprodutivo, o número de ovos eclodidos, o conteúdo de galactogênio e alterações histopatológicas eram avaliadas. O padrão reprodutivo nos moluscos controle e infectados evidenciou um comportamento alternante, nos quais períodos de alta produção de ovos e filhotes foram seguidos por períodos de baixa produção. No entanto, em relação ao conteúdo de galactogênio, moluscos controle e infectados seguiram o mesmo padrão de variação. Na histologia, observamos a presença de gametas masculinos e femininos com acentuada redução no número de óocitos. Os resultados indicam que o desenvolvimento intramolusco do parasito afeta a biologia reprodutiva do hospedeiro.

Reproductive Biology of Three Important Threatened/Near-Threatened Groupers (Plectropomus leopardus, Epinephelus polyphekadion and Plectropomus areolatus) in Eastern Indonesia and Implications for Management.

The three grouper species most heavily fished for the live reef fish trade (LRFT) in Indonesia are Plectopomus leopardus (greatest catch volume), and two species classified as Vulnerable on the International Union for Conservation of Nature (IUCN) Red List: Plectropomus areolatus and Epinephelus polyphekadion. Understanding the reproductive biology of these fishes is essential for sustainable management, but relevant data are limited. This study aimed to determine reproductive dynamics, so as to inform management measures to maintain the reproductive capacity of these groupers. Grouper gonad samples collected from fish caught for the LRFT were analyzed histologically. Data were also collected from participatory mapping and interviews with fishermen, and underwater monitoring of three known spawning aggregation sites in the Wakatobi National Park, Eastern Indonesia. Based on observed gonad development, the respective lengths and weights at first maturity were: 37.7 cm and 759 g (P. leopardus); 36.65 cm and 771.2 g (P. areolatus); 36.95 cm and 889.9 g (E. polyphekadion). The mean weight of the groupers market-based sampled was higher than the size at first sexual maturity. Sex transition was observed in P. leopardus; sex reversal was not observed in E. polyphekadion, and the sex pattern of P. areolatus was unresolved. Based on the fisher surveys and spawning aggregation monitoring, spawning occurs around the new moon from September to April, with reproductive peaks in November and December. Fisheries management measures that are suggested to sustain grouper stocks include enforcing appropriate size limits, temporal spatial closures (spawning aggregation sites), and a trading ban during the peak spawning season (November-December).

Seasonal and spatial variation in the reproductive biology of the dwarf seahorse Hippocampus zosterae.

Factors associated with the reproductive ecology of the dwarf seahorse Hippocampus zosterae were investigated. Fish from a Tampa Bay (FL, USA) seagrass ecosystem were collected, photographed and returned to the wild, with photos analysed to determine patterns of body size, density, sex ratio and reproductive state across site and season to understand the population dynamics of H. zosterae over time. Animal density did not vary significantly with site and season, indicating there is little evidence of seasonal migration in this species. Densities reported in this study were higher than the mean density for all seahorse species Hippocampus spp. There was no sexual dimorphism in body length and both sexes reached sexual maturity at the same size. The ratio of gravid to non-gravid males was found to shift by season but not by site, with breeding detected year-round in this population compared with populations further north in their range. Peak breeding (70% gravid males) was observed in the late summer-autumn (August-October) in the site furthest from shore. The largest fish for both sexes were recorded during the summer and autumn months in the mid-shore, deepest site. Sex ratio shifted by site with even sex ratios near the shore but significantly female-biased sex ratios detected at sites near open water. Lastly, an increase in marking dates with decreased time intervals between collections did not yield a higher recapture rate, compared with sampling in 2010. However, the Tampa Bay population of dwarf seahorses demonstrated stable densities across 3 years with year-round breeding, indicating that it is a robust population worthy of long-term monitoring for conservation efforts.

Evaluation of the reproductive profile of Subulina octona (Gastropoda, Subulinidae) experimentally infected by Paratanaisia bragai (Digenea, Eucotylidae)

Abstract Snails infected by trematodes may increase or decrease their reproductive activity in response to the presence of infection. Our aim was to verify the reproductive alterations in Subulina octona after infection by Paratanaisia bragai. The infected snails were individually exposed for 24 hours to 20 parasite eggs and four groups were formed (10, 20, 30 and 40 d.p.i.- days after infection), along with control groups. Every 10 days, the number of eggs in the reproductive tract, number of eggs hatched, galactogen content and histopathological changes were evaluated. The reproductive in the control and infected snails presented an alternating pattern, where periods of high production of eggs and newly hatched were followed by periods of low production. However, in relation to the amount of galactogen, both control and infected groups followed the same pattern of variation. In the histology, we observed the presence of male and female gametes with marked reduction in the number of oocytes. The results indicate that the intra-snail development of the parasite affects the reproductive biology of the host.

Resumo Moluscos infectados por trematódeos podem aumentar ou diminuir sua atividade reprodutiva em resposta à presença da infecção. Nosso objetivo foi verificar as alterações reprodutivas de Subulina octona após a infecção por Paratanaisia bragai. Os moluscos infectados foram individualmente expostos durante 24 horas a 20 ovos do parasito e quatro grupos foram formados (10, 20, 30 e 40 d.p.i. dias pós infecção), com respectivos grupos controle. A cada 10 dias, o número de ovos no trato reprodutivo, o número de ovos eclodidos, o conteúdo de galactogênio e alterações histopatológicas eram avaliadas. O padrão reprodutivo nos moluscos controle e infectados evidenciou um comportamento alternante, nos quais períodos de alta produção de ovos e filhotes foram seguidos por períodos de baixa produção. No entanto, em relação ao conteúdo de galactogênio, moluscos controle e infectados seguiram o mesmo padrão de variação. Na histologia, observamos a presença de gametas masculinos e femininos com acentuada redução no número de óocitos. Os resultados indicam que o desenvolvimento intramolusco do parasito afeta a biologia reprodutiva do hospedeiro.

Demography of some non-native isopods (Crustacea, Isopoda, Oniscidea) in a Mid-Atlantic forest, USA.

Introduced species dominate the terrestrial isopod fauna in most inland habitats of North America, including urban landscapes. These non-native species are often very abundant and thus potentially play a significant role in detritus processing. We monitored isopod assemblages in an urban forest for a year to examine the relationship between surface activity and abiotic environmental factors, and to analyze reproductive characteristics that might contribute to their successful establishment. Using pitfall trap samples we recorded five species, two of which, Trachelipusrathkii and Cylisticusconvexus, were highly abundant. We determined size, sex and reproductive state of each individual. Surface activity of both species reflected variability in abiotic stress factors for isopods, such as soil moisture and soil temperature. Early spring the main trigger was soil temperature while later in the season increasing temperature and decreasing soil moisture jointly affected population dynamics. Activity significantly correlated with soil moisture. The temporal pattern of sex ratios supported the secondary sex ratio hypothesis. Males dominated the samples on the onset of the mating season in search of females. The pattern was reversed as females searched for suitable microsites for their offspring. Size independent fecundity decreased as conditions became more stressful late in the season.

Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis.

Phylogenetic analyses indicate that viviparity (live-bearing reproduction) has originated independently in more than 150 vertebrate lineages, including a minimum of 115 clades of extant squamate reptiles. Other evolutionary origins of viviparity include 13 origins among bony fishes, nine among chondrichthyans, eight in amphibians, one in Paleozoic placoderms, six among extinct reptiles, and one in mammals. The origins of viviparity range geologically from the mid-Paleozoic through the Mesozoic to the Pleistocene. Substantial matrotrophy (maternal provision of nutrients to embryos during pregnancy) has arisen at least 33 times in these viviparous clades, with most (26) of these origins having occurred among fishes and amphibians. Convergent evolution in patterns of matrotrophy is widespread, as reflected by multiple independent origins of placentotrophy, histotrophy, oophagy, and embryophagy. Specializations for nutrient transfer to embryos are discontinuously distributed, reflecting the roles of phylogenetic inertia, exaptation (preadaptation), and constraint. Ancestral features that function in gas exchange and nutrition repeatedly and convergently have been co-opted for nutrient transfer, often through minor modification of their components and changes in the timing of their expression (heterochrony). Studies on functional and evolutionary morphology continue to play a central role in our attempts to understand viviparity and mechanisms of fetal nutrition.

Diversity of age-specific reproductive rates may result from ageing and optimal resource allocation.

This paper reports the results of a dynamic programming model which optimizes resource allocation to growth, reproduction and repair of somatic damage, based on the disposable soma theory of ageing. Here it is shown that different age-dependent patterns of reproductive rates are products of optimal lifetime strategies of resource partitioning. The array of different reproductive patterns generated by the model includes those in which reproduction begins at the maximum rate at maturity and then declines to the end of life, or increases up to a certain age and then drops. The observed patterns reflect optimal resource allocation shaped by the level of extrinsic mortality. A continuous decline in the reproductive rate from the start of reproduction is associated with high extrinsic mortality, and an early increase in the reproductive rate occurs under low extrinsic mortality. A long-lived organism shows a low reproductive rate early in life, and short-lived organisms start reproduction at the maximum rate.

Reproductive patterns in galagos (Galago zanzibaricus and Galago garnettii) in relation to climatic variability.

The reproductive patterns (birth seasonality, litter size, litters per year) of two sympatric species of galago (Galago zanzibaricus and G. garnettii) were studied in a coastal forest in Kenya for a two-year period. Trap-retrap and radio tracking methods were employed. G. zanzibaricus has one infant twice per year; G. garnettii has one infant once per year. Both species are seasonal breeders. These East African galagos are intermediate in reproductive patterns when compared with galagos from South African woodland (G. senegalensis moholi and G. crassicaudatus umbrosis) and West African rainforest (G. alleni and G. demidovii). Climatic patterns (total annual rainfall, seasonal variability of rainfall, variability in total annual rainfall, and annual temperature variability) are also compared for the three regions. Climatically, East Africa is intermediate between West and South Africa in total annual rainfall and in seasonality of rainfall, but not in year-to-year variability in rainfall. East Africa shows the highest variability in annual rainfall. South Africa has the coldest dry seasons and highest variability in temperatures. The results of this study suggest that "r-selection" and "K-selection" do not provide adequate explanations of galago reproductive patterns.