Anthropogenic land-use change decreases pollination and male and female fitness in terrestrial flowering plants.

BACKGROUND AND AIMS: The majority of the earth's land area is currently occupied by humans. Measuring how terrestrial plants reproduce in these pervasive environments is essential for understanding their long-term viability and their ability to adapt to changing environments. METHODS: We conducted hierarchical and phylogenetically-independent meta-analyses to assess the overall effects of anthropogenic land-use changes on pollination, and male and female fitness in terrestrial plants. KEY RESULTS: We found negative global effects of land use change (i.e., mainly habitat loss and fragmentation) on pollination and on female and male fitness of terrestrial flowering plants. Negative effects were stronger in plants with self-incompatibility (SI) systems and pollinated by invertebrates, regardless of life form and sexual expression. Pollination and female fitness of pollination generalist and specialist plants were similarly negatively affected by land-use change, whereas male fitness of specialist plants showed no effects. CONCLUSIONS: Our findings indicate that angiosperm populations remaining in fragmented habitats negatively affect pollination, and female and male fitness, which will likely decrease the recruitment, survival, and long-term viability of plant populations remaining in fragmented landscapes. We underline the main current gaps of knowledge for future research agendas and call out not only for a decrease in the current rates of land-use changes across the world but also to embark on active restoration efforts to increase the area and connectivity of remaining natural habitats.

Gametophytic self-incompatibility in Maxillariinae orchids.

Gametophytic self-incompatibility (GSI) has been mainly described in species-rich clades within Orchidaceae. We report GSI for a genus within Maxillariinae, one of the most conspicuous and diverse subtribes of neotropical orchids. Here, we describe the reproductive system of Brasiliorchis picta, B. phoenicanthera, and B. porphyrostele. Anatomical studies of fruit development showed that pollen tubes of aborted, self-pollinated flowers degenerate half-way in the stylar channel and never reach the ovules. Spontaneous self-pollination and emasculation set no fruits for none of the sampled species, thus supporting the hypothesis that these three species studied rely on the agency of pollinators and pollinator-mediated cross-pollination to set fruit. Fruit set from cross-pollinations ranged from 33.4 to 77.5%. One self-pollinated fruit of B. porphyrostele developed to completion. All other fruits aborted between 10 and 21 days after pollination. These data support previous evidence of variable strength GSI being exhibited in orchid species. Additional studies of self-incompatibility systems are needed to evaluate their role in species diversification and evolution of reproductive strategies in Maxillariinae and to allow for effective conservation strategies of threatened orchid species.

Alternative Evolutionary Pathways in Paspalum Involving Allotetraploidy, Sexuality, and Varied Mating Systems.

The genetic systems of Paspalum species have not been extensively studied. We analyzed the ploidy, reproductive mode, mating system, and fertility of four Paspalum species-Paspalum durifolium, Paspalum ionanthum, Paspalum regnellii, and Paspalum urvillei. An analysis of 378 individuals from 20 populations of northeastern Argentina was conducted. All populations of the four Paspalum species were pure tetraploid and had a sexual and stable reproductive mode. However, some populations of P. durifolium and P. ionanthum showed low levels of apospory. Populations of P. durifolium and P. ionanthum had low seed sets under self-pollination but were fertile under open pollination, showing that self-incompatibility likely caused self-sterility. In contrast, populations of P. regnellii or P. urvillei showed no evidence of apospory, and seed sets in both self- and open pollination conditions were high, suggesting that they are self-compatible due to the absence of pollen-pistil molecular incompatibility mechanisms. The evolutionary origin of the four Paspalum species could explain these differences. This study supplies valuable insights into the genetic systems of Paspalum species, which could have implications for their conservation and management.

A review of the reproductive system in anuran amphibians.

Reproductive biology is an important topic that is well explored in many vertebrates, but information about frogs' reproductive mechanisms could be improved. Therefore, this review aims to provide organized and specific information on frog reproduction. First, we developed schemes that illustrate the general information regarding reproductive biological mechanisms in frogs in a specific way. Then, we described the physiological, histological, and morphological mechanisms of each organ of the reproductive system of male and female frogs. Finally, this manuscript may contribute to a broader understanding of anuran reproductive biology. Since, understanding frogs' reproductive system permits one to make a comparison with reproduction with other anurans.

First evidence of multiple paternity in the blue shark (Prionace glauca).

Multiple paternity (MP) is defined as the behaviour in which females successfully mate with multiple males leading to offspring from different sires within the same litter. MP seems to be frequent and an evolutionary advantage in elasmobranchs. Here the authors report for the first time the occurrence of MP in the cosmopolitan blue shark Prionace glauca L. The evidence, gathered via microsatellite genotyping of pregnant females and their embryos, suggests that MP is very frequent in this species. Knowledge of MP in P. glauca should help describe more precisely its reproductive biology and contribute to the management of its populations.

Latitudinal Variation in the Toxicity and Sexual Compatibility of Alexandrium catenella Strains from Southern Chile.

The bloom-forming toxic dinoflagellate Alexandrium catenella was first detected in southern Chile (39.5-55° S) 50 years ago and is responsible for most of the area's cases of paralytic shellfish poisoning (PSP). Given the complex life history of A. catenella, which includes benthic sexual cysts, in this study, we examined the potential link between latitude, toxicity, and sexual compatibility. Nine clones isolated from Chilean Patagonia were used in self- and out-crosses in all possible combinations (n = 45). The effect of latitude on toxicity, reproductive success indexes, and cyst production was also determined. Using the toxin profiles for all strains, consisting of C1, C2, GTX4, GTX1, GTX3, and NeoSTX, a latitudinal gradient was determined for their proportions (%) and content per cell (pg cell-1), with the more toxic strains occurring in the north (-40.6° S). Reproductive success also showed a latitudinal tendency and was lower in the north. None of the self-crosses yielded resting cysts. Rather, the production of resting cysts was highest in pairings of clones separated by distances of 1000-1650 km. Our results contribute to a better understanding of PSP outbreaks in the region and demonstrate the importance of resting cysts in fueling new toxic events. They also provide additional evidence that the introduction of strains from neighboring regions is a cause for concern.

Migration through a Major Andean Ecogeographic Disruption as a Driver of Genetic and Phenotypic Diversity in a Wild Tomato Species.

Evolutionary dynamics at the population level play a central role in creating the diversity of life on our planet. In this study, we sought to understand the origins of such population-level variation in mating systems and defensive acylsugar chemistry in Solanum habrochaites-a wild tomato species found in diverse Andean habitats in Ecuador and Peru. Using Restriction-site-Associated-DNA-Sequencing (RAD-seq) of 50 S. habrochaites accessions, we identified eight population clusters generated via isolation and hybridization dynamics of 4-6 ancestral populations. Detailed characterization of mating systems of these clusters revealed emergence of multiple self-compatible (SC) groups from progenitor self-incompatible populations in the northern part of the species range. Emergence of these SC groups was also associated with fixation of deleterious alleles inactivating acylsugar acetylation. The Amotape-Huancabamba Zone-a geographical landmark in the Andes with high endemism and isolated microhabitats-was identified as a major driver of differentiation in the northern species range, whereas large geographical distances contributed to population structure and evolution of a novel SC group in the central and southern parts of the range, where the species was also inferred to have originated. Findings presented here highlight the role of the diverse ecogeography of Peru and Ecuador in generating population differentiation, and enhance our understanding of the microevolutionary processes that create biological diversity.

The origin of the parrotfish species Scarus compressus in the Tropical Eastern Pacific: region-wide hybridization between ancient species pairs.

BACKGROUND: In the Tropical Eastern Pacific (TEP), four species of parrotfishes with complex phylogeographic histories co-occur in sympatry on rocky reefs from Baja California to Ecuador: Scarus compressus, S. ghobban, S. perrico, and S. rubroviolaceus. The most divergent, S. perrico, separated from a Central Indo-Pacific ancestor in the late Miocene (6.6 Ma). We tested the hypothesis that S. compressus was the result of ongoing hybridization among the other three species by sequencing four nuclear markers and a mitochondrial locus in samples spanning 2/3 of the latitudinal extent of the TEP. RESULTS: A Structure model indicated that K = 3 fit the nuclear data and that S. compressus individuals had admixed genomes. Our data could correctly detect and assign pure adults and F1 hybrids with > 0.90 probability, and correct assignment of F2s was also high in some cases. NewHybrids models revealed that 89.8% (n = 59) of the S. compressus samples were F1 hybrids between either S. perrico × S. ghobban or S. perrico × S. rubroviolaceus. Similarly, the most recently diverged S. ghobban and S. rubroviolaceus were hybridizing in small numbers, with half of the admixed individuals assigned to F1 hybrids and the remainder likely > F1 hybrids. We observed strong mito-nuclear discordance in all hybrid pairs. Migrate models favored gene flow between S. perrico and S. ghobban, but not other species pairs. CONCLUSIONS: Mating between divergent species is giving rise to a region-wide, multispecies hybrid complex, characterized by a high frequency of parental and F1 genotypes but a low frequency of > F1 hybrids. Trimodal structure, and evidence for fertility of both male and female F1 hybrids, suggest that fitness declines sharply in later generation hybrids. In contrast, the hybrid population of the two more recently diverged species had similar frequencies of F1 and > F1 hybrids, suggesting accelerating post-mating incompatibility with time. Mitochondrial genotypes in hybrids suggest that indiscriminate mating by male S. perrico is driving pre-zygotic breakdown, which may reflect isolation of this endemic species for millions of years resulting in weak selection for conspecific mate recognition. Despite overlapping habitat use and high rates of hybridization, species boundaries are maintained by a combination of pre- and post-mating processes in this complex.

Two Self-Incompatibility Sites Occur Simultaneously in the Same Acianthera Species (Orchidaceae, Pleurothallidinae).

In most species of Pleurothallidinae, the self-incompatibility site occurs in the stylar canal inside the column, which is typical of gametophytic self-incompatibility (GSI). However, in some species of Acianthera, incompatible pollen tubes with anomalous morphology reach the ovary, as those are obstructed in the column. We investigated if a distinct self-incompatibility (SI) system is acting on the ovary of A. johannensis, which is a species with partial self-incompatibility, contrasting with a full SI species, A. fabiobarrosii. We analyzed the morphology and development of pollen tubes in the column, ovary, and fruit using light, epifluorescence, and transmission electron microscopy. Our results show that the main reaction site in A. johannensis is in the stylar canal inside the column, which was also recorded in A. fabiobarrosii. Morphological and cytological characteristics of the pollen tubes with obstructed growth in the column indicated a process of programmed cell death in these tubes, showing a possible GSI reaction. In addition, partially self-incompatible individuals of A. johannensis exhibit a second SI site in the ovary. We suggest that this self-incompatibility site in the ovary is only an extension of GSI that acts in the column, differing from the typical late-acting self-incompatibility system recorded in other plant groups.

Integrative depiction of the male reproductive system of the commercial purple crab Homalaspis plana (Platyxanthidae): Structure and function.

The information available on structures and function of reproductive systems are female-biased in many animal groups and crabs are not an exception. However, knowledge about the male reproductive system can help us to understand evolutionary and ecological processes such as the mating system and mating behavior. This study focuses on an integrative description of the principal regions of the male reproductive system of the purple crab, Homalaspis plana, a commercially exploited crab from the southeastern Pacific. For this description a combination of morphological observation, gravimetric records, histological and histochemical techniques and biochemical analysis were used. Also, a gross description of the seminal receptacle of the female was performed. The male reproductive system of H. plana was highly extended and complex, with a great capacity to produce and store spermatophores and secrete, at least, two kinds of seminal fluids. Sperm production, sperm packaging in spermatophores, storage of spermatophores and seminal liquid secretion were functions localized in specific regions. The vasosomatic index was the highest recorded to date in crabs, symptomatic of a high investment in reproduction. All these traits allow identification of H. plana as an internal sperm plug producer, which matches well with the highly extensible seminal receptacle of females. The great quantity of seminal material transferred to females during mating indicates that males may be able to mate only one time in the reproductive season and thus this species could be vulnerable to sperm depletion in males and sperm limitation in females if the fishery substantively reduced the abundance of males in the populations.

Fluctuating selection strength and intense male competition underlie variation and exaggeration of a water strider's male weapon.

Sexually selected traits can reach high degrees of phenotypic expression and variation under directional selection. A growing number of studies suggest that such selection can vary in space, time and form within and between populations. However, the impact of these fluctuations on sexual trait evolution is poorly understood. In the water strider Microvelia longipes, males display striking trait exaggeration and phenotypic variation manifested as extreme differences in the rear leg length. To study the origin and maintenance of this exaggerated trait, we conducted comparative behavioural, morphometric and reaction norm experiments in a selection of Microvelia species. We uncovered differences both in the mating behaviour and the degree of sexual dimorphism across these species. Interestingly, M. longipes evolved a specific mating behaviour where males compete for egg-laying sites, consisting of small floating objects, to intercept and copulate with gravid females. Through male-male competition assays, we demonstrated that male rear legs are used as weapons to dominate egg-laying sites and that intense competition is associated with the evolution of rear leg length exaggeration. Field observations revealed rapid fluctuation in M. longipes habitat stability and the abundance of egg-laying sites. Paternity tests using genetic markers demonstrated that small males could only fertilize about 5% of the eggs when egg-laying sites are limiting, whereas this proportion increased to about 20% when egg-laying sites become abundant. Furthermore, diet manipulation and artificial selection experiments also showed that the exaggerated leg length in M. longipes males is influenced by both genetic and nutritional factors. Collectively, our results highlight how fluctuation in the strength of directional sexual selection, through changes in the intensity of male competition, can drive the exaggeration and phenotypic variation in this weapon trait.

Reproductive behaviour and concurrent sound production of Gulf grouper Mycteroperca jordani (Epinephelidae) at a spawning aggregation site.

The reproductive and acoustic behaviours of Gulf grouper Mycteroperca jordani were studied at a spawning aggregation site in the southern Gulf of California, México. In May 2015-2017, divers located and surveyed a spawning aggregation site within Cabo Pulmo National Park. Adult M. jordani conformed to a lek mating system in which large males formed territories over sand adjacent to a rocky reef that were spatially segregated from smaller females outside of courtship and spawning periods. Females moved into male territories during evening hours to spawn. Male courtship behaviours targeted a single female, included head shakes and burst rises and preceded pair spawning prior to sunset. Males and females displayed three shared colour phases, but four phases were sex-specific. During evening hours, courtship and spawning, both sexes exhibited sexual dichromatism concurrent with reproductive behaviours. The pair-spawning mating system and observations of bimodal size distributions by sex support previous claims of protogyny in the species. Males produced sounds during territorial patrols, courtship and spawning rushes, which corroborated the importance of acoustic communication within the behavioural repertoire associated with spawning. Long-term acoustic monitoring revealed increases in total sounds detected day-1 from March through June with diel increases (e.g., evenings) that may be indicative of the spawning season. Observations of spawning on 12 consecutive evenings in May 2017 coupled with extended periods of sound production suggest that spawning does not follow a lunar rhythm. This first description of the mating system and sounds of the endangered M. jordani facilitates future development of seasonal and areal protections to restore and manage the species.

Evolutionary consequences of ecological factors: pollinator reliability predicts mating-system traits of a perennial plant.

The reproductive-assurance hypothesis predicts that mating-system traits will evolve towards increased autonomous self-pollination in plant populations experiencing unreliable pollinator service. We tested this long-standing hypothesis by assessing geographic covariation among pollinator reliability, outcrossing rates, heterozygosity and relevant floral traits across populations of Dalechampia scandens in Costa Rica. Mean outcrossing rates ranged from 0.16 to 0.49 across four populations, and covaried with the average rates of pollen arrival on stigmas, a measure of pollinator reliability. Across populations, genetically based differences in herkogamy (anther-stigma distance) were associated with variation in stigmatic pollen loads, outcrossing rates and heterozygosity. These observations are consistent with the hypothesis that, when pollinators are unreliable, floral traits promoting autonomous selfing evolve as a mechanism of reproductive assurance. Extensive covariation between floral traits and mating system among closely related populations further suggests that floral traits influencing mating systems track variation in adaptive optima generated by variation in pollinator reliability.

Evolutionary routes to non-kin cooperative breeding in birds.

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection--when individuals increase their inclusive fitness by aiding genetic relatives--is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.

Behavioral ecology of Heteragrion consors Hagen (Odonata, Megapodagrionidae): a shade-seek Atlantic forest damselfly

Behavioral ecology of Heteragrion consors Hagen (Odonata: Megapodagrionidae): a shade-seek Atlantic forest damselfly. The intensity of the inter and intra-sexual selection can affect male behavioral traits as territorial fidelity and aggressiveness allowing the existence of different strategies. However, its differential success could be affected by environmental - as the diel variation in temperature - and physiological constrains - as the variation in thermoregulatory abilities. In this context, we present a behavioral analysis of Heteragrion consors (Zygoptera, Megapodagrionidae) trying to characterize its mating system, diel activity pattern, temporal budget, territoriality and reproductive biology. These data were obtained based on field observations using the focal individual method and mark-recapture techniques in 120 m of a shaded Atlantic Forest stream in Brazil. The males of this species were territorial, varying in its local fidelity, while the females appear sporadically. Males were perched in the majority of the time, but were also observed in cleaning movements, longitudinal abdominal flexion, wing flexion and sperm transfer during perch. The males presented a perched thermoregulatory behavior related to an exothermic regulation. Foraging and agonistic interactions were rare, but dominate the other behavioral activities. Abdominal movements associated to long lasting copula pointed to the existence of sperm competition in this species. Males performed contact post-copulatory guarding of the females. These observations pointed to a non-resource mating system for this species.

Ecologia comportamental de Heteragrion consors Hagen (Odonata: Megapodagrionidae): uma libélula de áreas sombreadas da Floresta Atlântica. A intensidade de seleção inter e intra-sexual deve afetar características comportamentais dos machos como fidelidade a territórios e agressividade possibilitando a existência de diferentes estratégias. No entanto, seu sucesso diferencial pode ser afetado por restrições ambientais, como a variação da temperatura durante o dia; e fisiológicas, como a capacidade de termoregulação. Neste contexto, apresentamos os resultados de uma análise do comportamento de Heteragrion consors (Zygoptera, Megapodagrionidae) buscando caracterizar seu sistema de acasalamento, padrão de atividade diário, orçamento temporal, territorialidade e biologia reprodutiva. Essas informações foram obtidas por observação em campo a partir do método de indivíduo focal e pela técnica de marcação-recaptura em 120 m de um riacho predominantemente sombreado de Floresta Atlântica no Brasil. Os machos desta espécie foram territoriais com variação na fidelidade local, enquanto as fêmeas praticaram visitas esporádicas. Machos permaneceram pousados durante a maior proporção do tempo, mas foram observados realizando movimentos de limpeza, flexão longitudinal abdominal, flexão alar e transferência espermática durante o pouso. A espécie apresentou comportamento termorregulatório do tipo empoleirador relacionado à regulação exotérmica. Forrageio e interações agonísticas foram raras, mas predominaram sobre as outras atividades comportamentais observadas. Movimentos abdominais associados a uma cópula de duração longa apontam para existência de competição espermática na espécie. Machos forneceram guarda pós-copulatória com contato as fêmeas. Estas observações apontam para um sistema de acasalamento não-baseado em recursos para esta espécie.

No size or density effect on alternative mate-locating tactics in the tropical damselfly Hetaerina rosea males (Odonata: Calopterygidae)

Males of the damselfly Hetaerina rosea may defend mating sites along river margins (resident males) or, alternatively, wander among different areas presumably searching for mates (nonterritorial males). Although the occurrence of territorial and nonterritorial males of H. rosea is very common in Brazil, studies examining which factors may be responsible for the adoption of alternative mate-locating tactics in this species are inexistent. We investigated the relationship between the adoption of these alternative mate-locating tactics by males of H. rosea and two possible causes: body weight and male abundance. We carried the study in three areas: sites 1, 2 and 3. Samples were monthly undertaken in sites 1 and 2 between September/2001 and August/2002 and in site 3 between May/1999 and January/2001. Using the scan method with fixed areas and mark-resighting techniques, we did not find any relationship between the proportion of nonterritorial males and male abundance per month on sites 2 (n=6) and 3 (n=7), indicating that the adoption of alternative mate-locating tactics is not affected by competition for territories. In the same way, nonterritorial and resident males showed similar body and thoracic weight measures (n=30 and n=27 for sites 2 and 3 respectively). Maybe the nonterritorial tactic is adopted by individuals searching for better territories or males that were evicted from their defended sites. The absence of relationship between weight and male territorial status is in accordance with other Hetaerina species. However, other traits not investigated here such as parasitic load, fat content and age may influence the adoption of different mate-acquisition tactics in H. rosea males. Rev. Biol. Trop. 57 (1-2): 361-370. Epub 2009 June 30.

Los machos de la libélula Hetaerina rosea pueden defender sus sitios de apareamiento a lo largo de márgenes de ríos (machos residentes) o, alternativamente, deambulan entre diferentes áreas presumiblemente buscando pareja (machos no territoriales). Aunque la existencia de machos territoriales y no territoriales de H. rosea es muy común en Brasil, no hay estudios que examinen cuáles factores pueden ser responsables para la adopción de tácticas alternativas para localizar pareja en esta especie. Investigamos la relación entre la adopción de estas tácticas alternativas para localizar pareja por machos de H. rosea, y dos posibles causas: peso del cuerpo y abundancia de machos. Realizamos el estudio en tres áreas: sitios 1, 2 y 3. Las muestras se tomaron mensualmente en sitios 1 y 2 entre setiembre 2001 y agosto 2002, y en sitio 3 entre mayo 1999 y enero 2001. La adopción de tácticas alternativas de localización de machos no se ve afectada por competencia por territorios. La ausencia de relación entre peso y estatus del macho territorial coincide con otras especies de Hetaerina. No obstante, otros rasgos que no fueron estudiados aquí, como la carga de parásitos, contenido de grasa y edad, pueden influenciar la adopción de diferentes tácticas de adquisición de pareja en machos de H. rosea.