Sndrome-floral-especializacion-y-status-sucesional-en-el-genero-ipomoea-en-la-Region-de-Chamela-Jalisco

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UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO 
POSGRADO EN CIENCIAS BIOLÓGICAS 
CENTRO DE INVESTIGACIONES EN ECOSISTEMAS 
 
SÍNDROME FLORAL, ESPECIALIZACIÓN Y STATUS SUCESIONAL EN EL 
GÉNERO IPOMOEA EN LA REGIÓN DE CHAMELA, JALISCO 
 
T E S I S 
QUE PARA OPTAR POR EL GRADO DE : 
DOCTOR EN CIENCIAS 
 
P R E S E N T A : 
VÍCTOR MANUEL ROSAS GUERRERO 
 
TUTOR PRINCIPAL DE TESIS: DR. MAURICIO RICARDO QUESADA AVENDAÑO 
 CENTRO DE INVESTIGACIONES EN ECOSISTEMAS 
COMITÉ TUTOR: DR. ALBERTO KEN OYAMA NAKAGAWA 
 CENTRO DE INVESTIGACIONES EN ECOSISTEMAS 
 DR. JUAN SERVANDO NÚÑEZ FARFÁN 
 INSTITUTO DE ECOLOGÍA 
 
MORELIA, MICHOACÁN ABRIL 2013 
 
UNAM – Dirección General de Bibliotecas 
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UN M~ 
POSG DO~. ~~ 
Ciencias 
Dr. Isidro Ávila Martínez 
Director General de Administración Escolar, UNAM 
Presente 
COORDINACiÓN 
Por medio de la presente me permito informar a usted que en la reunión ordinaria del Comité Académico del 
Posgrado en Ciencias Biológicas, celebrada el día 26 de octubre del 2009, se acordó poner a su 
consideración el siguiente jurado para el examen de DOCTOR EN CIENCIAS del alumno ROSAS 
GUERRERO VíCTOR MANUEL con número de cuenta 501004161, con la tesis titulada: "SíNDROME 
FLORAL, ESPECIALIZACiÓN Y STATUS SUCESIONAL EN EL GÉNERO Ipomoea EN LA REGiÓN DE 
CHAMELA, JALISCO", bajo la dirección del DR. MAURICIO RICARDO QUESADA AVENDAÑO. 
Presidente: 
Vocal : 
Secretario: 
Suplente: 
Suplente: 
Dr. Alberto Ken Oyama Nakagawa 
Dr. Alejandro Casas Fernández 
Dr. César Augusto Domínguez Pérez-Tejada 
Dr. José Guadalupe García Franco 
Dr. Juan Servando Núñez Farfán 
El Comité Académico, aprobó que la integración del jurado se realizara a solicitud del alumno, con cinco 
sinodales, acogiéndose al artículo QUINTO TRANSITORIO, con base en lo establecido en el Artículo 31 del 
Reglamento General de Estudios de Posgrado vigente. 
Sin otro particular, quedo de usted. 
ATENTAMENTE 
"POR MI RAZA HABLARA EL ESPIRITU" 
Cd . Universitaria, D.F., a 28 de febrero del 2013. 
If-lid ~ (1, Jl)' 
DRA. MARiA DEL CORO ARIZIi::: ARRIAGA 
COORDINADORA DEL PROGRAMA 
Edif. de Posgrado P. B. (Costado Sur de la Torre 11 de Humanidades) Ciudad Universitaria c.P. 04510 México, D.F. 
Tel. 5623-0173 Fax: 5623-0172 http://pcbiol.posgrado.unam.mx 
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“A mis 38 años de existencia, 
en la única verdad absoluta en la que todavía creo 
es que no existe tal” 
 
“La felicidad no radica en obtener todas las cosas que queremos 
si no en tener las pocas cosas que realmente necesitamos” 
 
“Descubrí que lo mejor de la vida existe después de la muerte … 
de nuestros dioses y dogmas” 
 
“La etapa más brillante de nuestra vida es la niñez, 
pues nuestra curiosidad se encuentra al máximo 
 y nuestra dependencia de algún dios al mínimo” 
 
“Lo más emocionante de realizar una investigación 
no es el hallar una respuesta 
sino el generar más preguntas” 
 
 
 
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Con profundo agradecimiento a: 
Centro de Investigaciones en Ecosistemas y al Posgrado en Ciencias Biológicas de 
la Universidad Nacional Autónoma de México por aceptarme en su programa de 
Doctorado en Ciencias y el apoyo para la culminación de este. 
 
Consejo Nacional de Ciencia y Tecnología y a la Dirección General de Estudios de 
Posgrado de la Universidad Nacional Autónoma de México y a Tropi-Dry por los 
diversos apoyos económicos recibidos a lo largo del proyecto de tesis. 
 
Mauricio Quesada Avendaño, Ken Oyama Nakagawa y Juan Núñez Farfán por toda 
su ayuda, consejos y asesoría durante todo el transcurso del proyecto de tesis. 
 
Alejandro Casas Fernández, César Domínguez Pérez Tejada, Juan Fornoni Agnelli 
y José García Franco por sus comentarios sobre la tesis e interés en el examen de 
candidatura. 
 
Lorena Alemán Figueroa (Milo), Lucero Ríos Díaz, Natalia Carrillo Reyna y Yunuén 
García Rojas por toda su invaluable ayuda en el trabajo de campo. 
 
Centro de Investigaciones en Ecosistemas y la estación de Biología de Chamela de 
la Universidad Nacional Autónoma de México y la Universidad de Portsmouth por 
la ayuda en mi formación académica y apoyo logístico. 
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Ramiro Aguilar, Lorena Alemán Figueroa, Scott Armbruster, Lorena Ashworth, 
Jesús Bastida, Martha Lopezaraiza Mikel, Silvana Martén Rodríguez, Rocío Pérez 
Barrales, Mauricio Quesada y Stacey DeWitt Smith por sus ideas, ayuda, 
comentarios y toda su colaboración para la elaboración de los manuscritos 
derivados de la tesis. 
 
Lilia Espinosa Sánchez, Lilia Jiménez Solís, María de Jesús Márquez Salazar y 
Armando Rodríguez Reyes de la Coordinación del Posgrado en Ciencias 
Biológicas; así como a Ireri Guzmán Piñón, Aida Moysén, Dolores Rodríguez 
Guzmán, Roberto Sayago Lorenzana y Alejandro Rebollar de la Unidad de 
Posgrado en el Centro de Investigaciones en Ecosistemas por su gran ayuda en 
todos los trámites administrativos. 
 
Todos los amigos del laboratorio por su grata compañía, tanto en Chamela como 
en el CIEco y su gran apoyo en los momentos difíciles: Maria de Jesús Aguilar 
(Marichuuujb;), Ramiro Aguilar (Ra), Lorena Ashworth (Lo), Mariana Álvarez 
(Marianuska), Luis Daniel Ávila (Lui), Francisco Balvino (Balvi), Jesús Bastida (Jesú), 
Nancy Calderón, Natalia Carrillo (Natalus), José Contreras (Yosé), Rogelio Cruz 
(Royelius), Paola Fernández (Pao), Yunuén García (Yuni-yuni-yuni), Martha 
Lopezaraiza (Martiuuux), Jacob Pérez (Jacó), Lucero Ríos (Luchero), Gloria 
Rodríguez (Gyoyia), Gumersindo Sánchez (Gumeeee), Octavio Sánchez (Octa), 
Roberto Sáyago (Mijo), Eugenia Sentíes (Euge), Silvia Solís (Golda), Isadora Torres 
(Iiiisa). 
 
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Con sincera dedicación a: 
Milo. Por ser mi ayudante incondicional, el pilar de mi vida, inspiración, devoción 
y mi complemento perfecto. Por todos los recuerdos inolvidable y hermosos que 
hemos vivido solos y con nuestros chamacos. Te súper amo. 
 
Milito y Nic. Por alegrarme todos los días desde que nacieron e iluminarme sobre 
lo que realmente importa en la vida. Los amo profundamente. 
 
Tita. Por todos tus cuidados, atenciones, ayuda incondicional y por todo el amor 
que he recibido de ti desde el inicio de mi vida. Por ser esa persona tan 
maravillosa que siempre ha estado a mi lado. Te quiero mucho. 
 
Betito. Por todo tu esfuerzo para que pudiera aprender y no tener que 
preocuparme por mis necesidades básicas desde mi formación básica hasta 
terminada mi carrera y por alentarme a aspirar siempre más allá. 
 
Burgui, Nena y Primo. Por ser mis mejores amigos desde toda la vida y ser los 
ejemplos a seguir en mi ruta interior y con los que me rodean. Son mis ídolos. Los 
amo mucho. 
 
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Índice 
Resumen ........................................................................................................................ 11
Abstract .........................................................................................................................15
Introducción general ...................................................................................................... 19
Papel de la especialización y el sistema de apareamiento en la variación e 
integración floral ..................................................................................... 21
Asociación entre caracteres florales y tipo de polinizador ............................. 22
Efecto de la sucesión secundaria en el ensamblaje de polinizadores ............. 24
Literatura citada ........................................................................................... 25
Capítulo I. Influencia de la especialización en la polinización y el sistema de apareamiento 
en la integración floral y variación fenotípica en Ipomoea ............................................... 29
Abstract .................................................................................................................. 30
INTRODUCTION ....................................................................................................... 31
MATERIALS AND METHODS ...................................................................................... 32
Study species and study site ......................................................................... 32
Pollination specialization .............................................................................. 32
Floral variation and covariation ..................................................................... 33
Testing the effects of breeding system on correlation and integration patterns
 ............................................................................................................... 34
Phylogenetic analyses of floral variation, correlation and integration ............. 34
RESULTS .................................................................................................................. 35
Floral visitors and pollination specialization .................................................. 35
Phenotypic variation in relation to pollination specialization ......................... 35
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Effects of pollination specialization on correlation and integration patterns .. 36
Effects of breeding system and pollination specialization on attraction and 
efficiency traits ........................................................................................ 37
DISCUSSION ............................................................................................................. 38
Patterns of phenotypic variation ................................................................... 38
Patterns of phenotypic covariation and floral integration .............................. 39
Influence of breeding system on floral integration ........................................ 40
Conclusions ................................................................................................. 41
ACKNOWLEDGMENTS ............................................................................................... 41
LITERATURE CITED ................................................................................................... 41
SUPPORTING INFORMATION ..................................................................................... 44
Capítulo II. Revisión de síndromes de polinización: ¿Los caracteres florales predicen los 
polinizadores efectivos? ................................................................................................. 45
Abstract .................................................................................................................. 47
Predicting pollination systems from pollination syndromes ...................................... 48
Empirical evidence of pollination syndromes ............................................................ 49
Reliability of pollination syndromes ......................................................................... 50
Traits associated with higher predictability of pollination syndromes ....................... 52
The role of secondary pollinators on pollinator shifts ............................................... 56
Evolution of pollination syndromes .......................................................................... 59
Conservation and evolutionary prospects ................................................................. 61
Conclusions and future directions ........................................................................... 62
Acknowledgments ................................................................................................... 64
References .............................................................................................................. 64
Figures .................................................................................................................... 69
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Capítulo III. Los síndromes florales predicen los polinizadores legítimos de Ipomoea ..... 75
INTRODUCTION ....................................................................................................... 79
MATERIALS AND METHODS ...................................................................................... 82
Study site and species .................................................................................. 82
Pollinator visitation ....................................................................................... 82
Floral traits ................................................................................................... 84
Assignation of pollination syndromes ........................................................... 85
Reliability of classic pollination syndromes in Ipomoea ................................. 85
Association between floral traits and pollinators ........................................... 86
RESULTS .................................................................................................................. 86
Floral syndromes and pollinator importance ................................................. 86
Floral traits associated with particular pollinators ......................................... 88
Reliability of pollination syndromes .............................................................. 89
DISCUSSION ............................................................................................................. 91
Reliability of pollination syndromes .............................................................. 92
Suites of floral traits associated with several pollination syndromes .............. 94
Main floral traits on floral divergence ........................................................... 96
Conclusions ................................................................................................. 97
ACKNOWLEDGEMENTS ............................................................................................. 98
LITERATURE CITED ................................................................................................... 99
TABLES .................................................................................................................. 105
FIGURES ................................................................................................................. 107
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Capítulo IV. Cambios en los ensamblajes de los polinizadores de Ipomoea wolcottiana 
(Convolvulaceae) en diferentes estadios de sucesión .................................................... 112
Materials and methods .......................................................................................... 117
Study site and study species ....................................................................... 117
Flower abundance ...................................................................................... 118
Pollinatorassemblages ............................................................................... 118
Results .................................................................................................................. 120
Flower abundance ...................................................................................... 120
Pollinator assemblages ............................................................................... 121
Visitation rates ........................................................................................... 121
Pollinator importance ................................................................................. 122
Pollinator specialization .............................................................................. 122
Discussion ............................................................................................................. 123
Floral visitor richness and composition ....................................................... 124
Pollinator specialization and most effective pollinators ............................... 125
Conclusions .......................................................................................................... 127
References ............................................................................................................ 128
Figures .................................................................................................................. 134
Discusión general ......................................................................................................... 143
Literatura citada ......................................................................................... 152
 
 
 
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RESUMEN 
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La selección mediada por los polinizadores en los caracteres florales debería 
reducir su variación fenotípica e incrementar las correlaciones entre dichos 
caracteres promoviendo la integración floral. Sin embargo, en plantas generalistas 
la consistencia de la selección en caracteres florales podría disminuir, provocando 
una reducción en la integración floral. Independientemente del nivel de 
generalización, se espera que las flores reflejen adaptación a aquellos visitantes 
que más incrementen su adecuación a través de una polinización efectiva. Si 
diferentes especies de plantas son visitadas por polinizadores similares, se 
esperaría que tales especies presentaran convergencias en sus caracteres florales. 
Por lo tanto, se esperaría que exista una asociación entre los caracteres florales y 
el tipo de polinizador, lo cual se conoce como síndromes florales. Sin embargo, 
esta idea ha sido cuestionada debido a la aparente generalización encontrada en 
muchas especies. Asimismo, dicha asociación podría ser inexistente en plantas en 
sitios perturbados, debido a que el polinizador al cual la planta está mejor 
adaptada podría ser vulnerable a la perturbación. 
En este estudio, evalué si el nivel de especialización y de dependencia de 
polinizadores en 22 especies del género Ipomoea podría influir sobre los patrones 
de variación de caracteres florales e integración floral. Además, examiné si existía 
una asociación entre el conjunto de caracteres florales y polinizadores en estas 
especies y si los caracteres florales podrían predecir a los polinizadores más 
efectivos de las plantas a través de una revisión cuantitativa de la literatura. 
Finalmente, determiné los cambios en el ensamblaje de polinizadores de una 
especie de ipomea generalista en sitios con distintos tiempos de perturbación, 
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para evaluar si el polinizador predicho por los síndromes se encontraba a lo largo 
de la sucesión o si presentaba algún polinizador alternativo en algún estadio. 
Los resultados muestran que las plantas especialistas y autocompatibles 
muestran menor variación en caracteres florales y mayor integración floral que las 
plantas generalistas o autoincompatibles. Además, los caracteres florales 
involucrados en la deposición y remoción de polen muestran menor variación y 
mayor integración que los caracteres asociados a la atracción de polinizadores. 
Estos resultados indican que los polinizadores y el sistema de apareamiento son 
determinantes en la variación floral fenotípica y promueven la integración floral de 
los caracteres involucrados en la deposición de polen en los estigmas más que la 
integración de todos los caracteres florales. 
Los resultados obtenidos en la revisión bibliográfica, así como en las 22 
especies de ipomea referidas, validan el concepto de síndromes florales, ya que se 
encontró que los polinizadores más efectivos generalmente eran los predichos 
por los síndromes y las plantas polinizadas por visitantes florales similares 
presentaban, a menudo caracteres florales semejantes. No obstante, se encontró 
que la capacidad de predicción de los síndromes florales es mayor en plantas 
tropicales y predominantemente exógamas, que en plantas extratropicales y 
autocompatibles. Estos resultados sugieren que las plantas tropicales 
experimentan una selección mediada por los polinizadores más consistente en los 
caracteres florales, y por tanto, un mayor ajuste entre polinizadores y caracteres 
florales. Esto podría deberse a que una mayor diversidad de especies y menor 
amplitud de nicho presente en los trópicos, favorezca el establecimiento de 
interacciones planta-polinizador más especializadas. Asimismo, los datos 
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sugieren que las plantas predominantemente exógamas presentan mayor presión 
de selección por sus polinizadores sobre los caracteres florales que las plantas 
menos dependientes de polinizadores (e.g. plantas autocompatibles). 
Finalmente, encontré un incremento progresivo desde estadios tempranos 
hasta tardíos, en el número de grupos funcionales y de especies de polinizadores 
de I. wolcottiana. Aún cuando las abejas exóticas fueron los polinizadores más 
importantes en todos los estadios sucesionales, las polillas fueron más efectivas 
en tocar anteras y estigmas. Debido a la relativa corta distancia de forrajeo de las 
abejas y a la gran producción de flores por día de I. wolcottiana las abejas podrían 
incrementar la geitonogamia, provocando una menor producción de frutos en esta 
planta autoincompatible. Sin embargo, al inicio de la sucesión las abejas podrían 
ser los únicos polinizadores de esta especie pionera, ya que las polillas parecen 
ser incapaces de persistir en dichos estadios. 
En conclusión, la selección mediada por los polinizadores es muy importante 
en la evolución floral, siendo particularmente relevante el papel del polinizador 
más efectivo. No obstante, dicha selección es más consistente en caracteres 
florales involucrados en la deposición y remoción de polen, así como en plantas 
especialistas y autocompatibles. Además, dicha presión parece ser esencial en la 
convergencia floral observada tanto en ipomeas como en muchas angiospermas, 
principalmente en aquellas ubicadas en regiones tropicales o con sistemas de 
apareamiento predominantemente exógamo. Finalmente, el número de especies y 
grupos funcionales de polinizadores puede aumentar conforme avance el estadio 
sucesional de la comunidad de plantas, lo cual podría provocar una disminución 
en la adecuación de las plantas presentes en estadios de sucesión temprana. 
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ABSTRACT 
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Natural selection mediated by pollinators on floral traits should reduce their 
phenotypic variation but also increase the correlations among these floral traits 
promoting floral integration. However, generalized pollination could decrease 
consistency in selection on particular floral traits, causing a reduction on floral 
integration.Independently of generalization level, it is expected that flowers 
reflect adaptation to those floral visitors that increase their fitness through 
effective pollination. If similar pollinators effect effective pollination in different 
plant species, it should be expected that they display floral convergence. Thus, it 
is expected that there exist an association among floral traits and the pollinator 
type, which is known as floral syndromes. However, this idea has been questioned 
given the apparent generalization founded in several plant species. Likewise, such 
association could disappear in plants at disturbed sites if their best adapted 
pollinator is vulnerable to habitat disruption. 
In this study, I evaluated whether the level of pollination specialization and 
pollinator dependence on 22 species of genus Ipomoea could influence 
phenotypic variation patterns on floral traits and floral integration. Furthermore, I 
tested whether there is an association between the suite of floral traits and the 
pollinators of these plant species and if the suite of floral traits could predict the 
most effective pollinators of plants through a global quantitative review of 
published literature. Finally, I determined the changes in pollinator assemblages 
of one species of ipomoea with generalized pollination in sites at different ages 
after habitat disturbance to evaluate whether the predicted pollinator by floral 
syndromes were founded at all successional stages or if this plant were visited by 
alternative pollinators at any stage. 
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The results showed that plants with specialized pollination and self-
compatibles displayed less phenotypic variation on floral traits and greater floral 
integration than generalist plants or self-incompatible species. Additionally, floral 
traits involved in pollen placement and pick up showed less variation and greater 
integration than floral traits involved in pollinator attraction. These results 
indicate that the pollinators and the breeding system of plants were important on 
floral phenotypic variation and promote floral integration on floral traits involved 
in pollen deposition on stigmas rather than on all floral traits. 
The results obtained in the quantitative review, as well as in the referred 22 
Ipomoea species, strongly support the pollination syndrome concept, since the 
most effective pollinators of plants frequently was the pollinator predicted by 
syndromes and since plants pollinated by similar floral visitors often showed 
similar floral traits. Nevertheless, the predictive capacity of floral syndromes is 
greater on tropical plants and in non-autogamous species than in extratropical 
and self-compatible plants. These results suggest that tropical plants experience 
a more consistent pollinator-mediated selective pressure on floral traits, and 
therefore, a greater fit between pollinators and floral traits. This could be due to 
the greater species richness and lower niche breadth presented in the tropics, 
which should favored the establishment of more specialized plant-pollinator 
interactions. Likewise, since non-autogamous plant species were highly 
dependent on pollinators to their reproductive success, they should display grater 
selective pressure by their pollinators on floral traits than less dependent-
pollinator plants (e.g. self-compatible or autogamous plant species). 
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Finally, I found a progressive increase in the number of functional groups 
and in the number of morphospecies of pollinators of I. wolcottiana from early to 
late successional stages. Even when non-native honeybees were the most 
important pollinators in all successional stages, hawkmoths were proportionately 
more effective at touching anthers and stigma than exotic and native bees. Given 
the relatively short forage distance of bees and the great production of flowers 
per day by I. wolcottiana, bees may increase geitonogamy, causing a lower fruit 
set in this self-incompatible tree. Nevertheless, at the beginning of the succession 
process, bees could be the only pollen vectors of this pioneer species, since 
hawkmoths seems to be unable to persist at earlier successional stages. 
In conclusion, pollinator-mediated selection is very important in floral 
evolution, mainly that driven by the most effective pollinator. However, this 
selection is more consistent in floral traits involved in pollen placement and pick 
up and in plants with specialized pollination and with self-compatibility system. 
Furthermore, pollinator-mediated selection is seems to be essential on the floral 
convergence observed in ipomeas as well as in angiosperms, mainly on those 
located in tropical regions and on plants predominantely exogamous. Finally, the 
number of species and functional groups of pollinators could increase along 
successional gradient, which could decrease fitness on plants at earlier 
succesional stages. 
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INTRODUCCIÓN GENERAL 
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La relación entre plantas y polinizador es una de las interacciones ecológicas más 
importantes, ya que la adecuación de las plantas depende en gran medida de ésta 
y, a su vez, los polinizadores a su vez dependen de las recompensas que las 
plantas les aportan [1]. Se ha estimado que la polinización mediada por animales 
contribuye a la reproducción sexual de alrededor del 87% de las especies de 
plantas con flor a nivel mundial, incrementándose hasta en un 94% en las regiones 
tropicales [2]. Aún cuando se desconoce el grado de dependencia de las plantas a 
los polinizadores para su reproducción, distintas revisiones de estudios sobre 
limitación de polen sugieren gran dependencia de polinizadores en muchas 
especies de plantas [3, 4], particularmente en especies tropicales [5, 6]. Esto 
sugiere a su vez, que en las angiospermas, la selección mediada por los 
polinizadores sobre los caracteres florales debe ocurrir frecuentemente [3]. 
Para un mayor entendimiento sobre el papel de los polinizadores en la 
selección de caracteres florales, es recomendable combinar estudios evolutivos y 
ecológicos de la interacción planta-polinizador. Por lo anterior, el presente 
estudio combina perspectivas de investigación ecológicas y evolutivas con el fin 
de analizar tres temas principales sobre la relación planta-polinizador: (1) el 
papel de la especialización y el sistema de apareamiento en la variación e 
integración floral, (2) la asociación entre los caracteres florales y el tipo de 
polinizador y (3) el efecto de la sucesión secundaria en el ensamblaje de 
polinizadores. Asimismo, se discute cómo los resultados de la presente 
investigación contribuyen al entendimiento de la evolución y ecología de esta 
interacción tan importante para el buen funcionamiento de los ecosistemas. 
Finalmente, se plantean algunas sugerencias para investigaciones futuras en este 
P á g i n a | 21 
 
 
 
 
 
apasionante campo de investigación. A continuación se describen con mayor 
detalle los tres temas principales del presente trabajo. 
 
Papel de la especialización y el sistema de apareamiento en la variación e 
integración floral 
Los caracteres florales que están bajo presión de selección mediada por 
polinizadores a menudo muestran menor variación genética y fenotípica [7, 8], así 
como una mayor correlación entre los caracteres que cumplan una función en 
común, es decir presentan una mayor integración floral [9-12]. Se espera que 
dicha variación sea menor y la integración mayor en plantas con polinización 
especialista que en plantas con polinización generalista, debido a una presión de 
selección más consistente en las primeras que en las últimas [13-15]. Asimismo, 
se espera que los caracteres florales involucrados en la deposición del polen en el 
estigma, y por tanto,en la adecuación de las plantas, deberían presentar menor 
variación y mayor integración que los caracteres involucrados principalmente en la 
atracción de los polinizadores [13, 16, 17]. Por otro lado, debido a que diversos 
autores consideran que la alta correlación entre caracteres florales es una 
condición ancestral [14, 18], también se espera que plantas con menor presión de 
selección mediada por polinizadores (e.g., plantas autocompatibles capaces de 
producir semillas de manera autónoma), presenten mayor nivel de integración y 
menor variación en caracteres florales que plantas más dependientes de 
polinizadores [14, 18]. 
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En el capítulo I, se examina el papel de los polinizadores y del sistema de 
apareamiento en la varianza e integración fenotípica floral en 20 especies de 
Ipomoea incorporando sus relaciones filogenéticas. Asimismo, se compararon los 
niveles de variación e integración entre caracteres florales relacionados con la 
atracción de polinizadores y caracteres involucrados en la deposición del polen en 
el estigma. Este es el primer estudio con información filogenética y observación 
directa de los polinizadores legítimos que evalúa la asociación entre la variación e 
integración floral con el sistema de apareamiento y el nivel de especialización en 
polinización. 
 
Asociación entre caracteres florales y tipo de polinizador 
Al examinar cómo las distintas características florales desempeñan un papel en la 
atracción de sus polinizadores aumentando el éxito reproductivo de las plantas 
que las presentan, se pueden identificar caracteres florales adaptativos a tipos 
particulares de polinizadores [19]. Stebbins [20] sostiene que las diversas 
estructuras florales y mecanismos de polinización de las angiospermas, 
representan radiaciones adaptativas a diferentes polinizadores, así como 
diferentes formas de adaptarse al mismo polinizador. Cuando taxa de 
angiospermas no relacionados utilizan los servicios de un mismo polinizador, a 
menudo convergen independientemente en conjuntos predecibles de 
características florales [21]. Faegri y van der Pijl [22, 23], formalizaron la 
caracterización de tales semejanzas planteando el concepto de síndromes florales 
(o síndromes de polinización), los cuales son un conjunto de características 
P á g i n a | 23 
 
 
 
 
 
florales (e.g., morfología, color, tamaño, olor, tipo y cantidad de recompensas), 
asociados con la atracción e interacción de un grupo específico de polinizadores 
[22, 24, 23]. Por ejemplo, las flores polinizadas por polillas están asociadas con 
apertura nocturna, color blanco, tubo floral profundo, flores en posición 
horizontal o “colgante”, gran cantidad de néctar y un fuerte olor dulce [22]. 
El concepto implica que los polinizadores se ordenen en grupos funcionales, 
los cuales se comporten de manera similar en la flor y ejerzan una presión de 
selección convergente sobre diversas características florales y que las plantas 
presenten polinización especializada por alguno de estos grupos [21]. Sin 
embargo, debido a la aparente generalización encontrada en numerosas especies 
de plantas (e.g., [25-30]), diversos autores han cuestionado que en realidad 
exista tal estrecha asociación entre características florales con grupos específicos 
de polinizadores (e.g., [31-39]). 
En los capítulos II y III se discute el concepto de síndromes florales, su 
utilidad como herramienta para predecir los polinizadores de las plantas, así 
como sus limitaciones y alcances en el entendimiento de la evolución y ecología 
de la interacción planta-polinizador. En el capítulo II se realiza una revisión 
exhaustiva de la literatura publicada sobre síndromes florales con el fin de 
explorar qué tan confiable puede ser la inferencia del polinizador más efectivo a 
partir de conocer las características florales de una planta. Asimismo, se examinó 
si la predictibilidad de los síndromes está asociada a la forma de vida, simetría 
floral, distribución geográfica, sistema de apareamiento y/o al tipo de polinizador 
de las plantas. Finalmente, se discute el papel de los polinizadores secundarios en 
la evolución de los síndromes florales, así como las implicaciones de éstos en la 
P á g i n a | 24 
 
 
 
 
 
ecología y conservación de la interacción planta-polinizador. Esta es la primera 
revisión cuantitativa sobre la predictibilidad de los síndromes florales. 
En el capítulo III se profundiza en el análisis de la asociación entre los 
caracteres florales de 22 especies de Ipomoea y sus polinizadores legítimos 
(visitantes florales que contactan anteras y estigmas) mediante dos 
aproximaciones: (1) probando si los síndromes clásicos utilizados en la literatura 
(descritos por van der Pijl y Faegri [22, 23]) permiten predecir de manera confiable 
los polinizadores legítimos y (2) probando si existe convergencia en rasgos 
florales en las plantas polinizadas por polinizadores pertenecientes al mismo 
grupo funcional. Este es el primer estudio que utiliza ambas aproximaciones para 
probar el marco conceptual de los síndromes de polinización en un grupo de 
plantas congenéricas con alta variedad de sistemas de polinización. 
 
Efecto de la sucesión secundaria en el ensamblaje de polinizadores 
La actividad humana ha transformado una gran proporción de la superficie 
terrestre, transformando la mayoría de los bosques maduros a campos de 
cultivos, potreros, minas, ciudades y parches de bosque secundario. Existe 
evidencia de que tales perturbaciones disminuyen la tasa de visitas y alteran la 
composición de los ensamblajes de los polinizadores [40-42]; sin embargo, se 
sabe poco acerca de cómo pueden cambiar las interacciones entre plantas y 
polinizadores a lo largo de gradientes sucesionales. Aún cuando más del 42% de 
los bosques tropicales del mundo son bosques secos [43, 44], todo el 
conocimiento sobre los cambios en los ensamblajes de polinizadores en distintos 
P á g i n a | 25 
 
 
 
 
 
estadios sucesionales proviene de estudios en bosques perennifolios o templados 
(e.g., [45, 46]). 
Debido a la alta tasa de deforestación y deficiente protección que ocurre 
actualmente en los bosques secos [47, 48], resulta crucial entender cómo las 
perturbaciones antropogénicas pueden alterar las interacciones entre plantas y 
polinizadores, y con base en esta información, diseñar programas de 
conservación apropiados. En el último capítulo de este trabajo, se compara la 
composición, riqueza y tasa de visitas de los polinizadores legítimos del árbol 
incompatible Ipomoea wolcottiana en tres diferentes estadios sucesionales, 
incluyendo el bosque maduro. Se espera que tanto el número de especies y de 
grupos funcionales de polinizadores, así como la tasa de vistas, aumenten 
conforme aumente el tiempo en que ocurrió la perturbación. Este es el primer 
estudio que evalúa a través de la observación directa de los polinizadores, los 
cambios en los ensamblajes de polinizadores a lo largo de un gradiente 
sucesional en los trópicos. 
La presente investigación aspira a contribuir al conocimiento científico sobre 
la evolución floral y la ecología de las interacciones entre plantas y sus 
polinizadores en las angiospermas. Asimismo, aspira a brindar elementos para el 
diseño de estrategias de conservación y restauración de ambientes perturbados. 
 
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P á g i n a | 29 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
CAPÍTULO I. INFLUENCIA DE LA ESPECIALIZACIÓN EN LA POLINIZACIÓN Y EL 
SISTEMA DE APAREAMIENTO EN LA INTEGRACIÓN FLORAL Y VARIACIÓN 
FENOTÍPICA EN IPOMOEA 
 
 
ORIGINAL ARTICLE
doi:10.1111/j.1558-5646.2010.01140.x
INFLUENCE OF POLLINATION SPECIALIZATION
AND BREEDING SYSTEM ON FLORAL
INTEGRATION AND PHENOTYPIC
VARIATION IN IPOMOEA
Vı́ctor Rosas-Guerrero,1,2 Mauricio Quesada,1,3 W. Scott Armbruster,4,5,6,7 Rocı́o Pérez-Barrales,4,8,9
and Stacey DeWitt Smith10,11
1Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Apartado Postal 27-3 (Xangari),
58089 Morelia, Michoacán, México
2E-mail: victor_rosas@yahoo.com
3E-mail: mquesada@oikos.unam.mx
4School of Biological Sciences, University of Portsmouth, Portsmouth, United Kingdom, PO1 2DY
5Institute of Arctic Biology, University of Alaska, Fairbanks, AK 99775, USA
6Deptartment of Biology, Norwegian University of Science and Technology, NO-7491, Trondheim, Norway
7E-mail: Scott.Armbruster@port.ac.uk
8Department of Plant Biology and Ecology, University of Seville, Seville 41080, Spain
9E-mail: Rocio.Barrales@port.ac.uk
10School of Biological Sciences, University of Nebraska, Lincoln, NE 68588-0118, USA
11E-mail: sdsmith@unl.edu
Received June 15, 2009
Accepted September 11, 2010
Natural selection should reduce phenotypic variation and increase integration of floral traits involved in placement of pollen
grains on stigmas. In this study, we examine the role of pollinators and breeding system on the evolution of floral traits by
comparing the patterns of floral phenotypic variances and covariances in 20 Ipomoea species that differ in their level of pollination
specialization and pollinator dependence incorporating phylogenetic relatedness. Plants with specialized pollination (i.e., those
pollinated by one functional group or by few morphospecies) displayed less phenotypic variation and greater floral integration
than generalist plants. Self-compatible species also displayed greater floral integration than self-incompatible species. Floral traits
involved in pollen placement and pick up showed less variation and greater integration than floral traits involved in pollinator
attraction. Analytical models indicate that both breeding system and the number of morphospecies had significant effects on floral
integration patterns although only differences in the former were significant after accounting for phylogeny. These results suggest
that specialist/self-compatible plants experience more consistent selection on floral traits than generalist/self-incompatible plants.
Furthermore, pollinators and breeding system promote integration of floral traits involved in pollen placement and pick up rather
than integration of the whole flower.
KEY WORDS: Developmental constraints, floral evolution, floral variation, phenotypic integration, plant-pollinator interaction,
self-compatibility.
3 5 0
C© 2010 The Author(s). Evolution C© 2010 The Society for the Study of Evolution.
Evolution 65-2: 350–364
INFLUENCE OF POLLINATORS ON FLORAL INTEGRATION
Traits under long-term directional or stabilizing selection are
expected to display reduced genetic and phenotypic variation
(Fisher 1958; Lande and Arnold 1983). Pollinator-mediated se-
lection can be an important factor shaping the patterns of varia-
tion and covariation of floral traits (Armbruster 1991; Armbruster
and Schwaegerle 1996; Cresswell 1998; Medel et al. 2003;
Armbruster et al. 2004; Pérez-Barrales et al. 2007; Pérez et al.
2007; Chalcoff et al. 2008; Ordano et al. 2008, but see Strauss
and Whittall 2006 and references therein). Natural selection im-
posed by pollinators should depend on the level of specializa-
tion in pollination relationships, being more consistent in plants
with specialized pollination than in plants with generalized pol-
lination (Herrera 1988, 1996; Fenster 1991; Armbruster et al.
1999). Several studies have demonstrated that species with floral
traits associated with specialized pollination (e.g., species with
zygomorphic flowers, species with long corolla tubes) have less
phenotypic variation within populations than species with traits
associated with generalized pollination (e.g., species with acti-
nomorphic flowers; Fenster 1991; Armbruster et al. 1999; Wolfe
and Krstolic 1999; Ushimaru et al. 2006; Meng et al. 2008).
Phenotypic selection studies in plants have usually focused
on the effect of single floral traits on plant fitness (reviewed by
Fenster et al. 2004). However, flowers are integrated units that may
require a precise configuration of floral organs for proper function
(Bissell and Diggle 2008). Thus, it is necessary to use multivariate
approaches to have a better understanding of the selective pres-
sure of pollinators on floral traits. Several authors proposed that
selection imposed by pollinators should favor the integration of
floral traits (i.e., correlations among traits within functional units)
(Berg 1960; Stebbins 1970; Conner and Via 1993; Armbruster and
Schwaegerle 1996; Armbruster et al. 1999, 2004; Murren 2002;
Anderson and Busch 2006; Ushimaru et al. 2006; Pérez-Barrales
et al. 2007). Also, selection for floral-trait correlations should
be more consistent in plants with specialized pollination than in
plants with generalized pollination (Berg 1960). However, previ-
ous studies that tested the influence of pollination specialization
on phenotypic variation and/or integration of floral traits, have
inferred pollination specialization either without direct observa-
tions of pollinators or without distinguishing between legitimate
pollinators and nonpollinating flower visitors, which could lead
to underestimate the role of true pollinators as selective agents
on floral traits (e.g., Berg 1960; Fenster 1991; Armbruster et al.
1999; Wolfe and Krstolic 1999; Ushimaru et al. 2006; Meng et al.
2008).
The magnitude of floral correlations could differ among flo-
ral traits with different functions. For example, it is expected that
floral traits that interact to favor accurate placement of pollen
grains on pollinators (e.g., stamen and style lengths), and thence
on stigmas, should be more correlated than floral traits that interact
to advertise floral rewards to pollinators (e.g., corolla diameter)
(Conner and Via 1993; Armbruster et al. 1999; Ordano et al.
2008). Floral traits related to efficient pollen delivery on stigmas
are more likely to directly affect plant fitness than floral traits
related to visitor attraction that may not result in legitimate pol-
lination. Additionally, floral traits related to advertisement could
attract both pollinators and floral antagonists (e.g., nectar robbers,
florivores), which could result in opposing selection on floral dis-
play (Strauss and Whittall 2006), causing less consistent selection
on attraction traits than on traits related to pollen placement and
pick up.
Floral-trait correlations could also differ among plant species
with different breeding system (Anderson and Busch 2006;
Pérez et al. 2007). Anderson and Busch (2006) found that self-
compatible Leavenworthia species have weaker stamen–pistil or
pistil–petal correlations, but similar stamen–pistil correlations
than self-incompatible Leavenworthia species. They suggested
that similar stamen–pistil correlations could be maintained by se-
lection to ensure self-pollination. Recently, Pérez et al. (2007)
showed that pollinator-dependent Schizanthus species exhibited
lower corolla integration than their autonomous selfingcongeners,
as well as a decoupling among nonfunctional traits and the rest
of the corolla traits. These authors suggested that species that
do not experience strong pollinator selection (i.e., autonomous
selfing species), should display high integration between all flo-
ral traits due to their genetic and developmental constraints and
due to a relaxed pollinator-mediated selection on nonfunctional
traits. If high covariation among all floral traits was the ancestral
condition, and nonfunctional traits are not under selection me-
diated by pollinators (Berg 1960; Pérez et al. 2007), we could
predict that self-compatible (SC) plants should exhibit stronger
correlations and greater floral integration among floral parts re-
lated to pollinator attraction (i.e., “non functional traits”) than
self-incompatible (SI) plants. Additionally, it could be expected
that SI plants should experience more consistent selection against
self-pollination than SC plants, promoting herkogamy (spatial
separation of anthers from stigma). These changes in positions of
stigmas or anthers can increase adaptive inaccuracy (deviation of
the population mean from its adaptive optimum) in pollen place-
ment on pollinators relative to stigma contact (Armbruster et al.
2004). Furthermore, it seems that higher inaccuracy in flowers is
related with lower levels of integration (Armbruster et al. 2009).
Therefore, it is expected that SI plants should display lower floral
integration than SC plants in both floral traits related to pollinator
attraction and floral traits related to pollen deposition.
Several studies have reported strong phenotypic correlations
among corolla tube, gynoecium, and androecium (Conner and
Via 1993; Conner and Sterling 1995; Faivre and McDade 2001;
Kudoh et al. 2001; Mayr and Weber 2006; Bissell and Dig-
gle 2008; Smith and Rausher 2008), but these patterns of phe-
notypic correlations may be caused by pleiotropy or linkage
EVOLUTION FEBRUARY 2011 3 5 1
VÍCTOR ROSAS-GUERRERO ET AL.
disequilibrium rather than correlational selection. For instance,
Conner (2002) demonstrated that after nine generations of en-
forced random mating, correlations between six floral traits in
wild radish plants were unchanged, showing that pleiotropy
generates these correlations. Smith and Rausher (2008) found
that the predicted response to selection for several floral traits
was substantially constrained by their genetic correlations. Thus,
developmental-genetic factors can slow or constrain the evolution
of the most advantageous combinations of traits by natural selec-
tion (Lande and Arnold 1983; Cheverud 1984; Smith et al. 1985;
Via and Lande 1985; Futuyma 1986; Zeng 1988; Arnold 1992;
Mitchell-Olds 1996; Conner 2002; Herrera et al. 2002; Hansen
et al. 2003; Caruso 2004; Anderson and Busch 2006; Bissell and
Diggle 2008; Smith and Rausher 2008).
Although distinguishing between the relative contribution
of natural selection and developmental-genetic constraints is a
recurrent question in evolutionary biology, most studies of phe-
notypic variation and covariation of floral traits have focused on
only one plant species (e.g., Armbruster 1991; Conner and Via
1993; Herrera 2001; Williams and Conner 2001; Conner 2002;
Herrera et al. 2002; Sanchez-Lafuente 2002; Brock and Weinig
2007; Frey 2007; Hansen et al. 2007; Pérez-Barrales et al. 2007)
or on several unrelated species (e.g., Berg 1960; Fenster 1991;
Armbruster et al. 1999; Wolfe and Krstolic 1999; Ushimaru et al.
2006; but see Armbruster et al. 2004). Genetic correlations caused
by pleiotropy are expected to be relatively similar across closely
related species, while selective pressures are expected to be
species-, or even population-specific (Conner and Sterling 1995;
Kudoh et al. 2001; Herrera et al. 2002). Thus, comparing the corre-
lation structure of flower traits in phylogenetically related species
with different breeding system or levels of pollination specializa-
tion should clarify the degree to which the correlation structure
among flower traits is influenced by developmental-genetic versus
ecological factors. Specifically, if developmental-genetic factors
generate patterns of phenotypic integration, then we expect to
see a strong phylogenetic signal in the distribution of integration
indices across species. Alternatively, if pollinator-mediated se-
lection largely generates patterns of phenotypic integration, then
we expect to detect considerable evolutionary lability and a weak
phylogenetic signal in degree of integration.
To determine whether pollinator-mediated selection or
developmental–genetic correlations alter patterns of floral phe-
notypic variance and integration, we studied 20 tropical species
of Ipomoea that differ in their degree of pollinator dependence
(i.e., self-compatible vs. self-incompatible) and in their pollina-
tor specialization (i.e., specialist vs. generalist, estimated as the
number of functional groups of pollinators and as the number of
pollinator morphospecies). In particular, we addressed the follow-
ing questions: (1) How much do these plant species differ in their
degree of pollinator specialization and pollinator dependence?,
(2) Do specialist species show less floral variation than generalist
species?, (3) Are there differences in patterns of correlation and
integration of floral traits among species with different degree of
pollinator specialization and pollinator dependence?, (4) Are flo-
ral traits that influence pollen removal and deposition (“efficiency-
function traits”) less variable, more strongly correlated and more
integrated than floral traits that relate to advertisement or ac-
cessibility to rewards (“attraction-function traits”)?, and (5) Are
present patterns of similarity in variation, correlation, and integra-
tion related to phylogenetic distance? To our knowledge, this is the
first study that tests in several closely related plant species across
a molecular phylogeny, the association of floral variation and/or
floral integration patterns with breeding system and pollination
specialization estimated through direct observation of legitimate
pollinators.
Materials and Methods
STUDY SPECIES AND STUDY SITE
The cosmopolitan genus Ipomoea (Convolvulaceae) comprises
approximately 650 species (Austin and Huáman 1996), with
the majority of species being tropical (Austin and Bianchini
1998). Ipomoea species commonly have pentamerous, actinomor-
phic, and gamopetalous flowers (McDonald 1991). Several types
of animals have been considered as pollinators, including bee-
tles, flies, bees, butterflies, moths, hummingbirds, and bats
(McDonald 1991; Chemás-Jaramillo and Bullock 2002; Galetto
and Bernardello 2004; Wolfe and Sowell 2006; Rosas-Guerrero
et al. unpubl. ms.).
Twenty species of Ipomoea were sampled in the tropical dry
forest of Chamela–Cuitzmala Biosphere Reserve on the Pacific
coast of Mexico (19◦30′N, 105◦03′W). These plant species show
great variation in flower color, time of flower opening, floral
shape, and breeding system (Chemás-Jaramillo and Bullock 2002;
Rosas-Guerrero et al. unpubl. ms.).
POLLINATION SPECIALIZATION
To estimate the level of pollination specialization, floral visitors
were recorded during three consecutive flowering seasons (from
August to March 2005–2008) using camcorders (Sony Digital
Handycam DCR-PC 100, DCR-TRV80E, DCR-SR42) during six
intervals of 30 m uniformly distributed along flower duration (i.e.,
from flower opening to flower wilt). We considered pollinators
those floral visitors that made contact with both anthers and stig-
mas. Each floral visitor was classified into a functional group
(sensu Armbruster et al. 2000) according to similarities in their
fit to, and behavior on, flowers. Members of a functional group
are expected to exert similar selection pressures on floral traits
(Fenster et al. 2004). Through filming, we were able to iden-
tify the functionalgroup of pollinators and differentiate between
3 5 2 EVOLUTION FEBRUARY 2011
INFLUENCE OF POLLINATORS ON FLORAL INTEGRATION
several morphospecies of pollinators. On average, we filmed
14 flowers (∼40 h) per species. Morphospecies-accumulation
curves indicated that pollinator morphospecies leveled off after
29 h of observation for all species (results not shown).
We use two approaches to estimate the level of pollination
specialization: the number of pollinator morphospecies (as a con-
tinuous variable) and as specialist/generalist (as a categorical vari-
able). We considered arbitrarily plant species with specialized
pollination as those that were legitimately pollinated exclusively
by one functional group of pollinators, and plant species with
generalized pollination as those pollinated legitimately by more
than one functional group of pollinators.
FLORAL VARIATION AND COVARIATION
To determine floral phenotypic variation and covariation, the fol-
lowing floral traits were measured in situ using a digital caliper
(Mitutoyo Corp., Kawasaki, Japan) with 0.1 mm precision, using
one fresh flower per individual in approximately 45 individu-
als per species chosen at random: corolla diameter (CD), corolla
length (CL), throat diameter (TD), tube length (TL), style length
(SL), longest stamen (LS), and shortest stamen (SS) (see Fig. 1).
All flower measurements were performed by one person and with-
out prior knowledge of the expected pattern of trait covariation.
The coefficient of variation (CV) for each trait was calculated and
used as a standardized measure of floral-size variation. To test for
differences in floral variation among plants with different polli-
nation specialization, we compared the average CV of each floral
trait in specialized and generalized plant species using a Mann–
Whitney two-sample test. We also compared the mean CV of each
Figure 1. Schematic representation of a typical flower of
Ipomoea. Measured floral traits: CD = corolla diameter, CL =
corolla length, TD = throat diameter, TL = tube length, SL = style
length, LS = longest stamen, SS = shortest stamen.
floral trait across all species, to test if those floral traits related
in pollen deposition and pick up (i.e., SL, LS, SS) have lower
variation than floral traits related to pollinator advertisement or
floral traits related to accessibility to rewards by floral visitors
(i.e., CD, CL, TL, TD) using a Wilcoxon matched pairs test.
To assess whether the covariance architecture of flowers more
likely reflects developmental-genetic constraints or natural selec-
tion, we compared the patterns of floral trait correlations and
floral integration among species with different pollination spe-
cialization and different breeding system. After being natural-log
transformed, we calculated Pearson product-moment correlations
among floral traits for each plant species. We compared the aver-
age correlation coefficient of species with specialized pollination
with plants with generalized pollination with a two-sample t-test.
Estimates of means and 95% confidence intervals were obtained
by bootstrapping (n = 20,000 permutations in each test). Using
these same procedure, we compared the average correlation co-
efficient of floral traits related with pollen deposition and pick up
(i.e., TL, SL, LS, SS; hereafter named “efficiency correlation co-
efficient”), with the average correlation coefficient of floral traits
related with the attraction/restriction of floral visitors (i.e., CD,
CL, TL, TD; hereafter named “attraction correlation coefficient”).
Besides comparing correlation patterns with the categorical vari-
ables of pollination specialization, we tested if correlation coeffi-
cients of floral traits were correlated with the number of pollinator
morphospecies using Spearman rank correlation.
Phenotypic integration was estimated using the variance of
the eigenvalues of a correlation matrix through a principal com-
ponent analysis (Wagner 1984; Cheverud et al. 1989) of the floral
traits mentioned previously. Prior to analysis, all measurements
were log-transformed to approach normality and homoscedastic-
ity more closely. As species differed in sample size, a corrected
integration index was estimated (see Wagner 1984; Pérez-Barrales
et al. 2007). The integration index was expressed as a percentage
of the maximum possible value. We compared the average inte-
gration index of floral traits for plants with specialized pollination
with plants with generalized pollination with a two-sample t-test.
The significance of differences between means and confidence
intervals were also obtained by bootstrapping (n = 20,000 per-
mutations in each test). Additionally, we tested if floral integration
indices were correlated with the number of pollinator morphos-
pecies using Spearman rank correlation.
To detect differences between floral traits involved in pollen
placement and pick up (TL, SL, LS, SS) with floral traits related
to attraction or restriction to floral visitors (CD, CL, TL, TD), we
compared the two integration indices (hereafter named “efficiency
integration index” and “attraction integration index,” respectively)
with a two-sample t-test as described previously.
Hereafter, all bootstrapping estimations were calculated with
Data Pilot version 1.03 (Anonymous 2003), while additional
EVOLUTION FEBRUARY 2011 3 5 3
VÍCTOR ROSAS-GUERRERO ET AL.
statistical analyses were performed with SAS version 9.1.3 (SAS
2002) and MATLAB 7.7 (The Mathworks, Natick, MA).
TESTING THE EFFECTS OF BREEDING SYSTEM
ON CORRELATION AND INTEGRATION PATTERNS
Our study includes five self-incompatible species (Ipomoea am-
pullacea, I. bracteata, I. pes-caprae, I. trifida, and I. wolcottiana),
and 10 self-compatible species (Ipomoea alba, I. chamelana, I.
clavata, I. hederifolia, I. meyeri, I. muricata, I. nil, I. pedicellaris,
I. quamoclit, and I. triloba) (Chemás-Jaramillo and Bullock 2002;
Rosas-Guerrero V., unpubl. ms.). Because self-compatible plants
could experience strong selection on floral traits involved in pollen
placement and pick up, we compared the average coefficients of
correlation and integration of efficiency-, and attraction-function
traits of plants with self-compatible system (n = 10) with those
plants with self-incompatible breeding system (n = 5).
To test for the effect of breeding system, pollination spe-
cialization and number of pollinator morphospecies on attrac-
tion or efficiency integration, we performed a generalized linear
model using a Poisson distribution for the dependent variables and
the logarithmic function as a link function using the GENMOD
procedure (SAS 2002). The model used attraction or efficiency
integration index as response variables and breeding system, pol-
lination specialization, and number of pollinator morphospecies
as independent variables.
PHYLOGENETIC ANALYSES OF FLORAL VARIATION,
CORRELATION AND INTEGRATION
To determine whether pollinator-mediated selection versus
developmental–genetic correlations have stronger effects on
patterns of floral phenotypic variance and integration, we con-
ducted analyses that accounted for the shared phylogenetic his-
tory while estimating the effects of pollination specialization and
breeding system on floral trait variation and covariation. Many
approaches have been proposed for incorporating phylogenetic
effects into statistical analyses (e.g., Felsenstein 1985; Garland
et al. 1993; Martins and Hansen 1997), and the choice of method
depends on factors including the type of data to be analyzed (e.g.,
discrete or continuous), the parameter(s) to be estimated (e.g.,
relationships among traits, ancestral trait values), and the evo-
lutionary models to be considered (e.g., Brownian motion,
Ornstein–Uhlenbeck process). Here we employ phylogenetic gen-
eralized least squares (PGLS) to estimate whether differences in
pollination specialization and breeding system acrossIpomoea
species affect variation in individual floral traits (CV), correla-
tion among floral traits (CC), and floral integration indices (II).
PGLS was chosen for this application because it allows for easy
comparison of a range of evolutionary models and can be used
to consider both discrete and continuous variables (Martins and
Hansen 1997).
As with all comparative methods, PGLS requires an estimate
of the phylogeny with branch lengths. For this purpose, we com-
piled ITS sequences for 78 species and 2 outgroups (Table S1)
from previous studies of Ipomoea and its relatives (Miller et al.
1999, 2004; Manos et al. 2001). This sampling included 13 of the
20 species studied (Table S1); sequences were not available for
the remaining 7 species. Sequences were aligned with MEGA 4.0
(Tamura et al. 2007) and subsequently corrected manually. Poorly
aligned positions were identified using Gblocks software version
0.91b (Castresana 2000) and eliminated. Phylogenetic analysis
was performed using likelihood in RAxML-7.0.4 (Stamatakis
2006). A general time-reversible model of sequence evolution
with gamma-distributed rate heterogeneity and a proportion of
invariant sites (GTR + � + I) was used, and the single maximum
likelihood phylogeny was ultrametricized with nonparametric rate
smoothing in TreeEdit (http://tree.bio.ed.ac.uk/software/treeedit).
Finally, the tree was pruned to include only the 13 taxa for which
trait data was collected and transformed in a variance–covariance
matrix for PGLS using the R package ape (Paradis et al. 2004).
As an assessment of phylogenetic signal in the trait data, we
calculated the K statistic (Blomberg et al. 2003) for all of the con-
tinuous measures of floral trait variation using the picante package
(Kembel et al. 2010) in R. The K statistic uses the variance of the
standardized phylogenetically independent contrasts as a measure
of how well the tree fits the data given a Brownian motion model
of trait evolution. K values of 1 correspond to the amount of sim-
ilarity predicted by the phylogeny under Brownian motion while
lower values indicate less signal, that is, less similarity in trait
values among closely related species. The significance of K can
be tested by permuting the data across the tree and recomputing
K from the shuffled values (Blomberg et al. 2003). We used the
phylosignal function in picante with 1000 permutations to con-
duct a one-tailed test for signal. However, as phylogenetic signal
is difficult to detect with fewer than 20 species (Blomberg et al.
2003), we did not consider the results definitive and conducted
GLS analyses both with and without incorporating the phylogeny.
PGLS analyses were conducted using the program MEReg-
PHYSIG developed by Ives et al. (2007) for use in MATLAB.
The effects of pollination specialization (coded as 0/1, special-
ized/generalized), number of morphospecies and breeding system
(coded as 0/1, self-incompatible, or compatible) on continuously
varying values of CV, CC and II were estimated individually and
jointly using two models, ordinary least squares (OLS) and PGLS.
The OLS regression model is a standard nonphylogenetic analysis
and is equivalent to PGLS using a completely unresolved (star)
phylogeny. PGLS incorporates the variance–covariance matrix
built from the ML phylogeny and assumes that traits have evolved
along the phylogeny via Brownian motion (BM). PGLS using a
BM model and including an intercept (as in MERegPHYSIG) is
equivalent to independent contrasts (Rohlf 2001). Although other
3 5 4 EVOLUTION FEBRUARY 2011
INFLUENCE OF POLLINATORS ON FLORAL INTEGRATION
Figure 2. Coefficients of variation of seven floral traits for 20 species of Ipomoea with different pollination specialization. Floral trait
abbreviations as in Figure 1. Mean = average of the coefficients of variations of the seven floral traits. Lines above bars indicate
+1SE. Asterisks indicate significant differences after Mann–Whitney two sample test. ∗P < 0.10, ∗∗P < 0.05. Asterisks in square indicate
significant differences after phylogenetic corrected data.
models of trait evolution can be used with PGLS, the number of
species available for these analyses (13) reduces the capacity to
accurately measure phylogenetic signal and thus to select among
models (Blomberg et al. 2003). For each model, the statistical
significance of the effects of pollination and breeding system on
the floral trait variables was estimated by parametric bootstrap-
ping using 2000 simulated datasets (Ives et al. 2007). Model fit
was compared using a likelihood ratio test with one degree of
freedom (Lavin et al. 2008). By comparing models with no phy-
logeny (OLS) to models assuming strong effects of phylogeny
(PGLS with BM), we aim to assess the extent to which our results
depend on assumptions about the phylogenetic effect.
Results
FLORAL VISITORS AND POLLINATION
SPECIALIZATION
Many species of Ipomoea were pollinated primarily by one func-
tional group of pollinator. However, only five species were pol-
linated by exclusively one functional group and were classified
as pollinator specialists (Table S2). Three species were pollinated
exclusively by moths, one by bees, and one by hummingbirds.
We were able to differentiate between 56 morphospecies
of floral visitors that made contact with the reproductive parts
of flowers. The number of morphospecies registered per plant
species varied widely, from one to 15 (Table S2).
Visitation rates of pollinators also varied widely, from 0.04 in
I. alba to 22.23 visits/flower/h in I. pes-caprae. We found that self-
compatible plants received, in average, fewer pollinator visits than
self-incompatible plants (mean = 0.96 vs. 5.87 visits/flower/h)
(see Table S2 for values for each species).
PHENOTYPIC VARIATION IN RELATION
TO POLLINATION SPECIALIZATION
As predicted, all measured floral traits showed less phenotypic
variation (lower CVs) in plants pollinated by one functional
group than in plants pollinated by more than one functional group
(Fig. 2). However, these differences were significant (without phy-
logenetic correction) only for corolla length (U = 65, P = 0.016),
tube length (U = 60, P = 0.049), and longest stamen (U = 60,
P = 0.049), and marginally significant for shortest stamen
(U = 57, P = 0.088). We also observed a significant differ-
ence between specialized (one functional group) and generalized
(more than one functional group) species when the mean CVs of
all floral traits were taken together (U = 60, P = 0.049).
Pooling all study species, corolla and throat diameters were
more variable (larger CVs) than were the length of the styles,
longest stamens and shortest stamens (Z > 2.02, P < 0.050 for all
comparisons; no phylogenetic correction). In plants with one func-
tional group of pollinator, corolla and throat diameters showed
more variation than corolla length and the shortest-stamen length
(Z > 2.02, P < 0.050 for all comparisons), while in plants with
EVOLUTION FEBRUARY 2011 3 5 5
VÍCTOR ROSAS-GUERRERO ET AL.
more functional groups of pollinators, corolla and throat diameters
were more variable than style length and the longest-stamen length
(Z > 2.21, P < 0.03 for all comparisons). These results indicate
less variation in floral traits involved in pollen placement and pick
up than in traits involved in attraction, as predicted from theory.
Comparisons incorporating phylogenetic effects showed
similar trends as reported previously, although these findings were
significant less often (note reduction in sample size). Across ana-
lyses comparing floral trait CVs between generalized and special-
ized species, OLS (nonphylogenetic) models consistently fit the
data better than PGLS in line with the generally low phylogenetic
signal detected in the data (Table S3). Generalized species were
found to have significantly greater corolla length (CL) variation
than specialized species under the OLS model (Table